Scientific publications from the Retinal Stem Cell Research group

Conjunctival epithelial cells resist productive SARS-CoV-2 infection

Jackson RM, Hatton CF, Spegarova JS, Georgiou M, Collin J, Stephenson E, Verdon B, Haq IJ, Hussain R, Coxhead JM, Mudhar HS, Wagner B, Hasoon M, Davey T, Rooney P, Khan CMA, Ward C, Brodlie M, Haniffa M, Hambleton S, Armstrong L, Figueiredo F, Queen R, Duncan CJA, Lako M.
Stem Cell Reports. 2022 Jul 12;17(7):1699-1713.

pRB-Depleted Pluripotent Stem Cell Retinal Organoids Recapitulate Cell State Transitions of Retinoblastoma Development and Suggest an Important Role for pRB in Retinal Cell Differentiation

Rozanska A, Cerna-Chavez R, Queen R, Collin J, Zerti D, Dorgau B, Beh CS, Davey T, Coxhead J, Hussain R, Al-Aama J, Steel DH, Benvenisty N, Armstrong L, Parulekar M, Lako M.
Stem Cells Transl Med. 2022 Apr 29;11(4):415-433.

Human Retinal Organoids Provide a Suitable Tool for Toxicological Investigations: A Comprehensive Validation Using Drugs and Compounds Affecting the Retina

Dorgau B, Georgiou M, Chaudhary A, Moya-Molina M, Collin J, Queen R, Hilgen G, Davey T, Hewitt P, Schmitt M, Kustermann S, Pognan F, Steel DH, Sernagor E, Armstrong L, Lako M.
Stem Cells Transl Med. 2022 Mar 17;11(2):159-177.

Activation of autophagy reverses progressive and deleterious protein aggregation in PRPF31 patient-induced pluripotent stem cell-derived retinal pigment epithelium cells

Georgiou M, Yang C, Atkinson R, Pan KT, Buskin A, Molina MM, Collin J, Al-Aama J, Goertler F, Ludwig SEJ, Davey T, Lührmann R, Nagaraja-Grellscheid S, Johnson CA, Ali R, Armstrong L, Korolchuk V, Urlaub H, Mozaffari-Jovin S, Lako M.
Clin Transl Med. 2022 Mar;12(3):e759.

Pathophysiology of aniridia-associated keratopathy: Developmental aspects and unanswered questions

Latta L, Figueiredo FC, Ashery-Padan R, Collinson JM, Daniels J, Ferrari S, Szentmáry N, Solá S, Shalom-Feuerstein R, Lako M, Xapelli S, Aberdam D, Lagali N. Ocul Surf. 2021 Oct;22:245-266.

Conjunctival epithelial cells resist productive SARS-CoV-2 infection

Retinal organoids provide unique insights into molecular signatures of inherited retinal disease throughout retinogenesis.

Watson A, Lako M.
J Anat. 2022 Sep 29. doi: 10.1111/joa.13768

Commentary: Progressive accumulation of cytoplasmic aggregates in PRPF31 retinal pigment epithelium cells interferes with cell survival

Georgiou M, Atkinson R, Mozaffari-Jovin S, Lako M
Clinical and Translational Discovery (in press)

Incorporating microglia-like cells in human induced pluripotent stem cell-derived retinal organoids

Chichagova V, Georgiou M, Carter M, Dorgau B, Hilgen G, Collin J, Queen R, Chung G, Ajeian J, Moya-Molina M, Kustermann S, Pognan F, Hewitt P, Schmitt M, Sernagor E, Armstrong L, Lako M
Journal of Cellular and Molecular Medicine (in press)

Retinal pigment epithelium extracellular vesicles are potent inducers of age-related macular degeneration disease phenotype in the outer retina

Kurzawa-Akanbi M, Whitfield P, Burté F, Maria Bertelli P, Pathak V, Doherty M, Hilgen B, Gliaudelytė L, Platt M, Queen R, Coxhead J, Porter A, Öberg M, Fabrikova D, Davey T, Shyan Beh C, Georgiou M, Collin J, Boczonadi V, Härtlova A, Taggart M, Al-AamaJ, Korolchuk V, Morris CM, Guduric-Fuchs J, Steel DH, Medina RJ, Armstrong L and Lako M
Journal of Extracellular Vesicles (in press)

re-mRNA Processing Factors and Retinitis Pigmentosa: RNA Splicing and Beyond

Yang C, Georgiou M, Atkinson R, Collin J, Al-Aama J, Nagaraja-Grellscheid S, Johnson C, Ali R, Armstrong L, Mozaffari-Jovin S, Lako M.
P Front Cell Dev Biol. 2021 Jul 28;9:700276.

Age-related macular degeneration - biomarkers and therapies.

Kurzawa-Akanbi M, Lotery A, Steel DH, Lako M.
Regen Med. 2021 May;16(5):431-434. Doi; 10.2217/rme-2021-0059. Epub 2021 May 19.

Dissecting the Transcriptional and Chromatin Accessibility Heterogeneity of Proliferating Cone Precursors in Human Retinoblastoma Tumors by Single Cell Sequencing-Opening Pathways to New Therapeutic Strategies?

Collin J, Queen R, Zerti D, Steel DH, Bowen C, Parulekar M, Lako M.
Invest Ophthalmol Vis Sci. 2021 May 3;62(6):18. doi: 10.1167/iovs.62.6.18.

A single cell atlas of human cornea that defines its development, limbal progenitor cells and their interactions with the immune cells.

Collin J, Queen R, Zerti D, Bojic S, Dorgau B, Moyse N, Molina MM, Yang C, Dey S, Reynolds G, Hussain R, Coxhead JM, Lisgo S, Henderson D, Joseph A, Rooney P, Ghosh S, Clarke L, Connon C, Haniffa M, Figueiredo F, Armstrong L, Lako M.
Ocul Surf. 2021 Apr 16:S1542-0124(21)00021-5. doi: 10.1016/j.jtos.2021.03.010.

In the eye of the storm: SARS-CoV-2 infection and replication at the ocular surface?

Armstrong L, Collin J, Mostafa I, Queen R, Figueiredo FC, Lako M.
Stem Cells Transl Med. 2021 Jul;10(7):976-986. doi: 10.1002/sctm.20-0543.

Zerti D, Hilgen G, Dorgau B, Collin J, Ader M, Armstrong L, Sernagor E, Lako M.

Transplanted pluripotent stem cell-derived photoreceptor precursors elicit conventional and unusual light responses in mice with advanced retinal degeneration.
Stem Cells. 2021 Jul;39(7):882-896. doi: 10.1002/stem.3365.

IGFBPs mediate IGF-1's functions in retinal lamination and photoreceptor development during pluripotent stem cell differentiation to retinal organoids.

Zerti D, Molina MM, Dorgau B, Mearns S, Bauer R, Al-Aama J, Lako M.
Stem Cells. 2021 Apr;39(4):458-466. doi: 10.1002/stem.3331.

Revisiting the role of factor H in age-related macular degeneration: Insights from complement-mediated renal disease and rare genetic variants.

Tzoumas N, Hallam D, Harris CL, Lako M, Kavanagh D, Steel DHW.
Surv Ophthalmol. 2021 Mar-Apr;66(2):378-401. doi: 10.1016/j.survophthal.2020.10.008.

Recent Advances in Stem Cell Therapy for Limbal Stem Cell Deficiency: A Narrative Review.

Ghareeb AE, Lako M, Figueiredo FC.
Ophthalmol Ther. 2020 Dec;9(4):809-831. doi: 10.1007/s40123-020-00305-2.

Complement modulation reverses pathology in Y402H-retinal pigment epithelium cell model of AMD by restoring lysosomal function.

Cerniauskas E, Kurzawa-Akanbi M, Xie L, Hallam D, Moya Molina M, White K, Steel D, Doherty M, Whitfield P, Al-Aama J, Armstrong L, Kavanagh D, Lambris JD, Korolchuk V, Harris C and Lako M.
Stem Cells Transl Med 2020 Dec;9(12):1585-1603.

Co-expression of SARS-CoV-2 entry genes in the superficial adult human conjunctival, limbal and corneal epithelium suggests an additional route of entry via the ocular surface.

Collin J, Queen R, Zerti D, Dorgau B, Georgiou M, Djidrovski I, Hussain R, Coxhead JM, Joseph A, Rooney P, Lisgo S, Figueiredo F, Armstrong L, Lako M.
Ocul Surf. 2020 Jun 3:S1542-0124(20)30097-5.

HCA Lung Biological Network. SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes.

Sungnak W, Huang N, Bécavin C, Berg M, Queen R, Litvinukova M, Talavera-López C, Maatz H, Reichart D, Sampaziotis F, Worlock KB, Yoshida M, Barnes JL
Nat Med. 2020 May;26(5):681-687.

Room temperature shipment does not affect the biological activity of pluripotent stem cell-derived retinal organoids.

Georgiou M, Chichagova V, Hilgen G, Dorgau B, Sernagor E, Armstrong L, Lako M.
PLoS One. 2020 Jun 1;15(6):e0233860.

AAV-Mediated Gene Augmentation Therapy Restores Critical Functions in Mutant PRPF31+/- iPSC-Derived RPE Cells.

Brydon EM, Bronstein R, Buskin A, Lako M, Pierce EA, Fernandez-Godino R.
Mol Ther Methods Clin Dev. 2019 Nov 11;15:392-402.

Coculture techniques for modeling retinal development and disease, and enabling regenerative medicine.

Ghareeb AE, Lako M, Steel DH.
Stem Cells Transl Med. 2020 Aug 7. doi: 10.1002/sctm.20-0201.

Revisiting the role of factor H in age-related macular degeneration: Insights from complement-mediated renal disease and rare genetic variants.

Tzoumas N, Hallam D, Harris CL, Lako M, Kavanagh D, Steel DHW.
Surv Ophthalmol. 2020 Nov 4:S0039-6257(20)30146-6. doi: 10.1016/j.survophthal.2020.10.008. Online ahead of print. PMID: 33157112.

IGFBPs mediate IGF-1’s functions in retinal lamination and photoreceptor development during pluripotent stem cell differentiation to retinal organoids.

Zerti D, Molina MM, Dorgau B, Mearns S, Bauer R, Al-Aama J and Lako M.
Stem Cells (in press).

Understanding the complexity of retina and pluripotent stem cell derived retinal organoids with single cell RNA sequencing: current progress, remaining challenges and future prospective.

Zerti D, Collin J, Queen R, Cockell SJ, Lako M.
Curr Eye Res. 2019 Dec 3. doi: 10.1080/02713683.2019.1697453. [Epub ahead of print] PMID: 31794277

Quantification of the morphological characteristics of hESC colonies.

Orozco-Fuentes S, Neganova I, Wadkin LE, Baggaley AW, Barrio RA, Lako M, Shukurov A, Parker NG.
Sci Rep. 2019 Nov 26;9(1):17569. doi: 10.1038/s41598-019-53719-9. PMID: 31772193

Human iPSC differentiation to retinal organoids in response to IGF1 and BMP4 activation is line- and method-dependent.

Chichagova V, Hilgen G, Ghareeb A, Georgiou M, Carter M, Sernagor E, Lako M, Armstrong L.
Stem Cells. 2019 Nov 13. doi: 10.1002/stem.3116. [Epub ahead of print] PMID: 31721366

Developing a simple method to enhance the generation of cone and rod photoreceptors in pluripotent stem cell-derived retinal organoids.

Zerti D, Dorgau B, Felemban M, Ghareeb AE, Yu M, Ding Y, Krasnogor N, Lako M.
Stem Cells. 2019 Oct 31. doi: 10.1002/stem.3082. [Epub ahead of print] PMID: 31670434

Seeding hESCs to achieve optimal colony clonality.

Wadkin LE, Orozco-Fuentes S, Neganova I, Bojic S, Laude A, Lako M, Parker NG, Shukurov A.
Sci Rep. 2019 Oct 25;9(1):15299. doi: 10.1038/s41598-019-51897-0. PMID: 31653933

Differentiation of Retinal Organoids from Human Pluripotent Stem Cells.

Chichagova V, Dorgau B, Felemban M, Georgiou M, Armstrong L, Lako M.
Curr Protoc Stem Cell Biol. 2019 Sep;50(1):e95. doi: 10.1002/cpsc.95. PMID: 31479596

Systematic Comparison of Retinal Organoid Differentiation from Human Pluripotent Stem Cells Reveals Stage Specific, Cell Line, and Methodological Differences.

Mellough CB, Collin J, Queen R, Hilgen G, Dorgau B, Zerti D, Felemban M, White K, Sernagor E, Lako M.
Stem Cells Transl Med. 2019 Jul;8(7):694-706. doi: 10.1002/sctm.18-0267. Epub 2019 Mar 27. PMID: 30916455

Decellularised extracellular matrix-derived peptides from neural retina and retinal pigment epithelium enhance the expression of synaptic markers and light responsiveness of human pluripotent stem cell derived retinal organoids.

Dorgau B, Felemban M, Hilgen G, Kiening M, Zerti D, Hunt NC, Doherty M, Whitfield P, Hallam D, White K, Ding Y, Krasnogor N, Al-Aama J, Asfour HZ, Sernagor E, Lako M.
Biomaterials. 2019 Apr;199:63-75. doi: 10.1016/j.biomaterials.2019.01.028. Epub 2019 Jan 22. PMID: 30738336

An integrated transcriptional analysis of the developing human retina.

Mellough CB, Bauer R, Collin J, Dorgau B, Zerti D, Dolan DWP, Jones CM, Izuogu OG, Yu M, Hallam D, Steyn JS, White K, Steel DH, Santibanez-Koref M, Elliott DJ, Jackson MS, Lindsay S, Grellscheid S, Lako M.
Development. 2019 Jan 29;146(2). pii: dev169474. doi: 10.1242/dev.169474. PMID: 30696714

CRX Expression in Pluripotent Stem Cell-Derived Photoreceptors Marks a Transplantable Subpopulation of Early Cones.

Collin J, Zerti D, Queen R, Santos-Ferreira T, Bauer R, Coxhead J, Hussain R, Steel D, Mellough C, Ader M, Sernagor E, Armstrong L, Lako M.
Stem Cells. 2019 May;37(5):609-622. doi: 10.1002/stem.2974. Epub 2019 Jan 30. PMID: 30681766

Deconstructing Retinal Organoids: Single Cell RNA-Seq Reveals the Cellular Components of Human Pluripotent Stem Cell-Derived Retina.

Collin J, Queen R, Zerti D, Dorgau B, Hussain R, Coxhead J, Cockell S, Lako M.
Stem Cells. 2019 May;37(5):593-598. doi: 10.1002/stem.2963. Epub 2019 Jan 12. PMID: 30548510

Splicing factor PRPF31 retinitis pigmentosa (RP11) is caused by disrupted alternative splicing programmes for genes implicated in pre-mRNA splicing, cellular adhesion and ciliogenesis.

A, Zhu, L, Chichagova V, Basu B, Mozafari-Jovin S et al, Luehrmann R, Grellscheid SN, Johnson CA and Lako M.
Nature Communications 2018; 9(1):4234. doi: 10.1038/s41467-018-06448-y.
(https://www.ncbi.nlm.nih.gov/pubmed/30315276)

Human-Induced Pluripotent Stem Cells Generate Light Responsive Retinal Organoids with Variable and Nutrient-Dependent Efficiency.

Hallam D, Hilgen G, Dorgau B, Zhu L, Yu M, Bojic S, Hewitt P, Schmitt M, Uteng M, Kustermann S, Steel D, Nicholds M, Thomas R, Treumann A, Porter A, Sernagor E, Armstrong L, Lako M. Stem Cells. 2018 Jul 13. doi: 10.1002/stem.2883.
Stem Cells. 2018 Jul 13. doi: 10.1002/stem.2883.

Special Series: Transplantation of Stem Cells into the Eye.
Lako M.

Stem Cells. 2018 Aug 22. doi: 10.1002/stem.2896. [Epub ahead of print] No abstract available.

Extracellular matrix component expression in human pluripotent stem cell-derived retinal organoids recapitulates retinogenesis in vivo and reveals an important role for IMPG1 and CD44 in the development of photoreceptors and interphotoreceptor matrix.

Felemban M, Dorgau B, Hunt NC, Hallam D, Zerti D, Bauer R, Ding Y, Collin J, Steel D, Krasnogor N, Al-Aama J, Lindsay S, Mellough C, Lako M.
Acta Biomater. 2018 Jul 1;74:207-221. doi: 10.1016/j.actbio.2018.05.023.

Laminin γ3 plays an important role in retinal lamination, photoreceptor organisation and ganglion cell differentiation.

Dorgau B, Felemban M, Sharpe A, Bauer R, Hallam D, Steel DH, Lindsay S, Mellough C, Lako M.
Cell Death Dis. 2018 May 23;9(6):615. doi: 10.1038/s41419-018-0648-0.

Cellular regeneration strategies for macular degeneration: past, present and future.

Chichagova V, Hallam D, Collin J, Zerti D, Dorgau B, Felemban M, Lako M, Steel DH.
Eye (Lond). 2018 May;32(5):946-971. doi: 10.1038/s41433-018-0061-z. Epub 2018 Mar 5. Review.

The Application of Biomaterials to Tissue Engineering Neural Retina and Retinal Pigment Epithelium.

Hunt NC, Hallam D, Chichagova V, Steel DH, Lako M.
Adv Healthc Mater. 2018 Sep 2:e1800226. doi: 10.1002/adhm.201800226. [Epub ahead of print] Review.

Human induced pluripotent stem cell and animal models of X-linked retinitis pigmentosa identify impaired gelsolin activation as a cause of photoreceptor loss.

Megaw E, Abu-Arafeh H, Mellough C, Gurniak-Witke C, Witke W, Dhillon B, Wright AF, Lako M and Ffrench-Constant C. (2017)
Nature Communications: 8:271.

Human iPSC disease modelling reveals functional and structural defects in retinal pigment epithelial cells harbouring the m.3243A>G mitochondrial DNA mutation.

Chichagova V, Hallam D, Collin J, Buskin A, Saretzki G, Armstrong L, Yu-Man P, Lako M and Steel D (2017)
Scientific Reports 26: 12320.

An iPSC patient specific model of CFH (Y402H) polymorphism displays characteristic features of AMD and indicates a beneficial role for UV light exposure. Stem Cells 35: 2305-2320.

Hallam D, Collin J, Bojic S, Chichagova V, Buskin A, Yu X, Lafage L, Otten EG, Anyfantis G, Mellough C, Przyborski S, Alharthi S, Korolchuk V, Lotery A, Saretzki G, McKibbin M, Armstrong L, Steel D, Lako M. (2017)

3D culture of human pluripotent stem cells in RGD - alginate hydrogel improves retinal tissue development. Acta Biomaterilia 49: 329-343.

Hunt NC, Hallam D, Karimi A, Mellough CB, Steel DHW and Lako M. (2017)

CHCHD2 primes the differentiation potential of human induced pluripotent stem cells to neuroectodermal lineages.

Zhu L, Gomez A, Saretzki G, Jin S, Tilgner K, Melguzo-Sanchiz D, Anyfantis G, Al-Aama J, Vallier L, Chinnery P, Lako M and Armstrong L (2016)
J. Cell Biology 215(2):187-202.

Using zinc finger nuclease technology to generate CRX-GFP reporter human embryonic stem cells as a tool to identify and study the emergence of photoreceptor precursors during pluripotent stem cell differentiation.

Collin J, Mellough CB, Dorgau B, Pryzborki S, Moreno-Gimeno I and Lako M (2016)
Stem Cells 34: 311-21 (Cover page image)

How to build a human.

Mellough CB and Lako M (2016)
Elife. 24;5. pii: e19826.

Tissue engineering using pluripotent stem cells: multidisciplinary approaches to accelerate bench-to-bedside transition.

Hunt NC and Lako M (2016)
Regen Med. 6:495-8.

Generation of Human Induced Pluripotent Stem Cells Using RNA-Based Sendai Virus System and Pluripotency Validation of the Resulting Cell Population.

Chichagova V, Sanchez-Vera I, Armstrong L, Steel D, Lako M. (2016)
Methods Mol Biol. 1353:285-307.

IGF-1 signalling plays an important role in the formation of three dimensional laminated neural retina and other ocular structures from human embryonic stem cells.

Mellough CB, Collin J, Khazim M, White K, Sernagor E, Steel D and Lako M (2015)
Stem Cells 33:2416-30.

Use of induced pluripotent stem cells technology to understand photoreceptor cytoskeletal dynamics in retinitis pigmentosa.

Megaw R, Mellough C, WRIGHT A, Lako M and Ffrench-Constant C (2015)
Lancet Suppl 1:S69. doi: 10.1016/S0140-6736(15)60384-1.

Lab generated retina: Realising the dream.

Mellough CB, Collin J, Sernagor E, Wride NK, Steel DH and Lako M (2014)
Vision Neuroscience 22:1-16.

Efficient stage-specific differentiation of human pluripotent stem cells towards retinal photoreceptor cells.

Mellough CB, Sernagor E, Moreno-Gimeno, I, Steel DHW and Lako M (2012)
Stem Cells 30:673-86 9.

Editorial: Our top 10 developments in stem cell biology over the last 30 years.

Armstrong L, Lako M, Buckley N, Lappin TR, Murphy MJ, Nolta JA, Pittenger M, Stojkovic M (2012).
Stem Cells. 30:2-9.
https://www.ncbi.nlm.nih.gov/pubmed/22162299

Concise review: putting a finger on stem cell biology: zinc finger nuclease-driven targeted genetic editing in human pluripotent stem cells.

Collin J, Lako M. (2011)
Stem Cells. 29:1021-33.

Human induced pluripotent stem cell lines show stress defense mechanisms and mitochondrial regulation similar to those of human embryonic stem cells.

Armstrong L, Tilgner K, Saretzki G, Atkinson SP, Stojkovic M, Moreno R, Przyborski S, Lako M.(2010)
Stem Cells. 28:661-73.

Induced pluripotent stem cells : it looks simple but can looks deceive?

Lako M, Armstrong L, Stojkovic M (2010).
Stem Cells.28:845-50.

Genetic basis of inherited macular dystrophies and implications for stem cell therapy.

Mellough CB, Steel DH, Lako M. (2009)
Stem Cells. 27(11):2833-45.