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Whole RNA-seq analysis reveals longitudinal proteostasis network responses to photoreceptor outer segment trafficking and degradation in RPE cells

Whole RNA-seq analysis reveals longitudinal proteostasis network responses to photoreceptor outer segment trafficking and degradation in RPE cells
Whole RNA-seq analysis reveals longitudinal proteostasis network responses to photoreceptor outer segment trafficking and degradation in RPE cells
RNA-seq analysis of the highly-differentiated human retinal pigment epithelial (RPE) cell-line ARPE-19, cultured on transwells for ≥4 months yielded 44,909 genes showing 83.35% alignment with the human reference genome. These included mRNA transcripts of RPE-specific genes and those involved in retinopathies. Monolayers were fed photoreceptor outer segments (POS), designed to be synchronously internalised, mimicking a homeo-static RPE activity. Cells were subsequently fixed at 4, 6, 24 and 48 hours when POS were previously shown to maximally co-localise with Rab5, Rab7, LAMP/lysosomes and LC3b/autophagic compartments. A comprehensive analysis of differentially expressed genes involved in proteolysis revealed a pattern of gene orchestration consistent with POS breakdown in the autophagy-lysosomal pathway. At 4 hours, these included elevated up-stream signalling events promoting early stages of cargo transport and endosome maturation, compared to RPE without POS exposure. This transcriptional landscape altered from 6 hours, transitioning to promoting cargo degradation in autolysosomes by 24-48 hours. Longitudinal scrutiny of mRNA transcripts revealed nuanced differences even within linked gene networks. POS exposure also initiated transcriptional upregulation in ubiquitin proteasome and chaperone-mediated systems within 4-6 hours, providing evidence of cross-talk with other proteolytic processes. These findings show detailed evidence of transcriptome-level responses to cargo trafficking and processing in RPE cells.
retinal pigment epithelium (RPE), RNA-seq, photoreceptor outer segments (POS), trafficking, proteostasis, age-related macular degeneration (AMD), inherited retinal dystrophies
2073-4409
Miller, Rebecca D.
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Mondon, Isaac
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Ellis, Charles
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Muir, Anna Marie
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Turner, Stephanie
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Keeling, Eloise
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Wai, Htoo A.
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Chatelet, David S.
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Johnson, David A.
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Tumbarello, David A.
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Lotery, Andrew J.
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Baralle, Diana
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Ratnayaka, J. Arjuna
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Miller, Rebecca D.
55f92938-8417-4e07-a482-8fa4f5da42e5
Mondon, Isaac
4108dfce-4c31-4c7f-89ab-5a554cc46510
Ellis, Charles
507f9816-974d-4cb7-9053-91ed67cd51b8
Muir, Anna Marie
3bb9296c-28a5-4c92-94c6-81d68115276a
Turner, Stephanie
82c85e82-755b-402e-bc14-751c14fdc8c3
Keeling, Eloise
3207bbdb-d391-44af-8abc-a60c08dce45b
Wai, Htoo A.
4428517b-33b3-42cb-9818-ca64763ab7bc
Chatelet, David S.
62e830df-81a7-489f-82e5-0576ccb99e18
Johnson, David A.
16f11035-d193-4315-a6c1-22ffbe8efe31
Tumbarello, David A.
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Lotery, Andrew J.
5ecc2d2d-d0b4-468f-ad2c-df7156f8e514
Baralle, Diana
faac16e5-7928-4801-9811-8b3a9ea4bb91
Ratnayaka, J. Arjuna
002499b8-1a9f-45b6-9539-5ac145799dfd

Miller, Rebecca D., Mondon, Isaac, Ellis, Charles, Muir, Anna Marie, Turner, Stephanie, Keeling, Eloise, Wai, Htoo A., Chatelet, David S., Johnson, David A., Tumbarello, David A., Lotery, Andrew J., Baralle, Diana and Ratnayaka, J. Arjuna (2025) Whole RNA-seq analysis reveals longitudinal proteostasis network responses to photoreceptor outer segment trafficking and degradation in RPE cells. Cells, 14 (15), [1166]. (doi:10.3390/cells14151166).

Record type: Article

Abstract

RNA-seq analysis of the highly-differentiated human retinal pigment epithelial (RPE) cell-line ARPE-19, cultured on transwells for ≥4 months yielded 44,909 genes showing 83.35% alignment with the human reference genome. These included mRNA transcripts of RPE-specific genes and those involved in retinopathies. Monolayers were fed photoreceptor outer segments (POS), designed to be synchronously internalised, mimicking a homeo-static RPE activity. Cells were subsequently fixed at 4, 6, 24 and 48 hours when POS were previously shown to maximally co-localise with Rab5, Rab7, LAMP/lysosomes and LC3b/autophagic compartments. A comprehensive analysis of differentially expressed genes involved in proteolysis revealed a pattern of gene orchestration consistent with POS breakdown in the autophagy-lysosomal pathway. At 4 hours, these included elevated up-stream signalling events promoting early stages of cargo transport and endosome maturation, compared to RPE without POS exposure. This transcriptional landscape altered from 6 hours, transitioning to promoting cargo degradation in autolysosomes by 24-48 hours. Longitudinal scrutiny of mRNA transcripts revealed nuanced differences even within linked gene networks. POS exposure also initiated transcriptional upregulation in ubiquitin proteasome and chaperone-mediated systems within 4-6 hours, providing evidence of cross-talk with other proteolytic processes. These findings show detailed evidence of transcriptome-level responses to cargo trafficking and processing in RPE cells.

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Accepted/In Press date: 25 July 2025
Published date: 29 July 2025
Keywords: retinal pigment epithelium (RPE), RNA-seq, photoreceptor outer segments (POS), trafficking, proteostasis, age-related macular degeneration (AMD), inherited retinal dystrophies

Identifiers

Local EPrints ID: 504798
URI: http://eprints.soton.ac.uk/id/eprint/504798
ISSN: 2073-4409
PURE UUID: 41daae13-79d7-47f4-a756-9e91612196ac
ORCID for Rebecca D. Miller: ORCID iD orcid.org/0000-0001-8550-6921
ORCID for Eloise Keeling: ORCID iD orcid.org/0000-0003-0399-359X
ORCID for Htoo A. Wai: ORCID iD orcid.org/0000-0002-3560-6980
ORCID for David A. Tumbarello: ORCID iD orcid.org/0000-0002-5169-0561
ORCID for Andrew J. Lotery: ORCID iD orcid.org/0000-0001-5541-4305
ORCID for Diana Baralle: ORCID iD orcid.org/0000-0003-3217-4833
ORCID for J. Arjuna Ratnayaka: ORCID iD orcid.org/0000-0002-1027-6938

Catalogue record

Date deposited: 18 Sep 2025 17:16
Last modified: 19 Sep 2025 02:05

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Contributors

Author: Rebecca D. Miller ORCID iD
Author: Isaac Mondon
Author: Charles Ellis
Author: Anna Marie Muir
Author: Stephanie Turner
Author: Eloise Keeling ORCID iD
Author: Htoo A. Wai ORCID iD
Author: David S. Chatelet
Author: David A. Johnson
Author: Diana Baralle ORCID iD

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