Exploring the human lacrimal gland using organoids and single-cell sequencing

The lacrimal gland is essential for lubrication and protection of the eye. Disruption of lacrimal fluid production, composition, or release results in dry eye, causing discomfort and damage to the ocular surface. Here, we describe the establishment of long-term 3D organoid culture conditions for mou...

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Published inCell stem cell Vol. 28; no. 7; pp. 1221 - 1232.e7
Main Authors Bannier-Hélaouët, Marie, Post, Yorick, Korving, Jeroen, Trani Bustos, Marc, Gehart, Helmuth, Begthel, Harry, Bar-Ephraim, Yotam E., van der Vaart, Jelte, Kalmann, Rachel, Imhoff, Saskia M., Clevers, Hans
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.07.2021
Subjects
adult stem cells
lacrimal gland
organoids
regeneration
single-cell sequencing
swelling assay
tear gland
tear secretion
transplantation
single-cell sequencing
regeneration
organoids
transplantation
swelling assay
lacrimal gland
tear secretion
tear gland
adult stem cells
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Abstract The lacrimal gland is essential for lubrication and protection of the eye. Disruption of lacrimal fluid production, composition, or release results in dry eye, causing discomfort and damage to the ocular surface. Here, we describe the establishment of long-term 3D organoid culture conditions for mouse and human lacrimal gland. Organoids can be expanded over multiple months and recapitulate morphological and transcriptional features of lacrimal ducts. CRISPR-Cas9-mediated genome editing reveals the master regulator for eye development Pax6 to be required for differentiation of adult lacrimal gland cells. We address cellular heterogeneity of the lacrimal gland by providing a single-cell atlas of human lacrimal gland tissue and organoids. Finally, human lacrimal gland organoids phenocopy the process of tear secretion in response to neurotransmitters and can engraft and produce mature tear products upon orthotopic transplantation in mouse. Together, this study provides an experimental platform to study the (patho-)physiology of the lacrimal gland. [Display omitted] •Derivation of adult stem cell-based organoids from mouse and human lacrimal gland•Pax6 is essential to maintain lacrimal gland duct identity in adult cells•Single-cell transcriptome analysis of major human lacrimal gland cell types•Lacrimal gland organoids can be induced to cry and are transplantable Lacrimal gland biology remains poorly understood. Here, we establish organoids from mouse and human lacrimal gland that can serve as study subjects for the lacrimal gland in vitro. In addition, we describe the human lacrimal gland at the single-cell level, which provides a platform for future studies.
AbstractList The lacrimal gland is essential for lubrication and protection of the eye. Disruption of lacrimal fluid production, composition, or release results in dry eye, causing discomfort and damage to the ocular surface. Here, we describe the establishment of long-term 3D organoid culture conditions for mouse and human lacrimal gland. Organoids can be expanded over multiple months and recapitulate morphological and transcriptional features of lacrimal ducts. CRISPR-Cas9-mediated genome editing reveals the master regulator for eye development Pax6 to be required for differentiation of adult lacrimal gland cells. We address cellular heterogeneity of the lacrimal gland by providing a single-cell atlas of human lacrimal gland tissue and organoids. Finally, human lacrimal gland organoids phenocopy the process of tear secretion in response to neurotransmitters and can engraft and produce mature tear products upon orthotopic transplantation in mouse. Together, this study provides an experimental platform to study the (patho-)physiology of the lacrimal gland.The lacrimal gland is essential for lubrication and protection of the eye. Disruption of lacrimal fluid production, composition, or release results in dry eye, causing discomfort and damage to the ocular surface. Here, we describe the establishment of long-term 3D organoid culture conditions for mouse and human lacrimal gland. Organoids can be expanded over multiple months and recapitulate morphological and transcriptional features of lacrimal ducts. CRISPR-Cas9-mediated genome editing reveals the master regulator for eye development Pax6 to be required for differentiation of adult lacrimal gland cells. We address cellular heterogeneity of the lacrimal gland by providing a single-cell atlas of human lacrimal gland tissue and organoids. Finally, human lacrimal gland organoids phenocopy the process of tear secretion in response to neurotransmitters and can engraft and produce mature tear products upon orthotopic transplantation in mouse. Together, this study provides an experimental platform to study the (patho-)physiology of the lacrimal gland.
The lacrimal gland is essential for lubrication and protection of the eye. Disruption of lacrimal fluid production, composition, or release results in dry eye, causing discomfort and damage to the ocular surface. Here, we describe the establishment of long-term 3D organoid culture conditions for mouse and human lacrimal gland. Organoids can be expanded over multiple months and recapitulate morphological and transcriptional features of lacrimal ducts. CRISPR-Cas9-mediated genome editing reveals the master regulator for eye development Pax6 to be required for differentiation of adult lacrimal gland cells. We address cellular heterogeneity of the lacrimal gland by providing a single-cell atlas of human lacrimal gland tissue and organoids. Finally, human lacrimal gland organoids phenocopy the process of tear secretion in response to neurotransmitters and can engraft and produce mature tear products upon orthotopic transplantation in mouse. Together, this study provides an experimental platform to study the (patho-)physiology of the lacrimal gland. [Display omitted] •Derivation of adult stem cell-based organoids from mouse and human lacrimal gland•Pax6 is essential to maintain lacrimal gland duct identity in adult cells•Single-cell transcriptome analysis of major human lacrimal gland cell types•Lacrimal gland organoids can be induced to cry and are transplantable Lacrimal gland biology remains poorly understood. Here, we establish organoids from mouse and human lacrimal gland that can serve as study subjects for the lacrimal gland in vitro. In addition, we describe the human lacrimal gland at the single-cell level, which provides a platform for future studies.
The lacrimal gland is essential for lubrication and protection of the eye. Disruption of lacrimal fluid production, composition, or release results in dry eye, causing discomfort and damage to the ocular surface. Here, we describe the establishment of long-term 3D organoid culture conditions for mouse and human lacrimal gland. Organoids can be expanded over multiple months and recapitulate morphological and transcriptional features of lacrimal ducts. CRISPR-Cas9-mediated genome editing reveals the master regulator for eye development Pax6 to be required for differentiation of adult lacrimal gland cells. We address cellular heterogeneity of the lacrimal gland by providing a single-cell atlas of human lacrimal gland tissue and organoids. Finally, human lacrimal gland organoids phenocopy the process of tear secretion in response to neurotransmitters and can engraft and produce mature tear products upon orthotopic transplantation in mouse. Together, this study provides an experimental platform to study the (patho-)physiology of the lacrimal gland.
Author Post, Yorick
Gehart, Helmuth
Clevers, Hans
Bar-Ephraim, Yotam E.
Trani Bustos, Marc
Korving, Jeroen
Imhoff, Saskia M.
Bannier-Hélaouët, Marie
Begthel, Harry
Kalmann, Rachel
van der Vaart, Jelte
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  surname: Korving
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  organization: Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences (KNAW), University Medical Center Utrecht, 3584 CT Utrecht, the Netherlands
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  givenname: Marc
  surname: Trani Bustos
  fullname: Trani Bustos, Marc
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  surname: Begthel
  fullname: Begthel, Harry
  organization: Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences (KNAW), University Medical Center Utrecht, 3584 CT Utrecht, the Netherlands
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  givenname: Yotam E.
  surname: Bar-Ephraim
  fullname: Bar-Ephraim, Yotam E.
  organization: Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences (KNAW), University Medical Center Utrecht, 3584 CT Utrecht, the Netherlands
– sequence: 8
  givenname: Jelte
  surname: van der Vaart
  fullname: van der Vaart, Jelte
  organization: Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences (KNAW), University Medical Center Utrecht, 3584 CT Utrecht, the Netherlands
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  givenname: Rachel
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  givenname: Saskia M.
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  fullname: Imhoff, Saskia M.
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  email: h.clevers@hubrecht.eu
  organization: Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences (KNAW), University Medical Center Utrecht, 3584 CT Utrecht, the Netherlands
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Keywords single-cell sequencing
regeneration
organoids
transplantation
swelling assay
lacrimal gland
tear secretion
tear gland
adult stem cells
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Snippet The lacrimal gland is essential for lubrication and protection of the eye. Disruption of lacrimal fluid production, composition, or release results in dry eye,...
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SubjectTerms adult stem cells
lacrimal gland
organoids
regeneration
single-cell sequencing
swelling assay
tear gland
tear secretion
transplantation
Title Exploring the human lacrimal gland using organoids and single-cell sequencing
URI https://dx.doi.org/10.1016/j.stem.2021.02.024
https://www.ncbi.nlm.nih.gov/pubmed/33730555
https://www.proquest.com/docview/2502807361
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