Adaptation to ex vivo culture reduces human hematopoietic stem cell activity independently of the cell cycle Article Swipe
Carys Johnson
,
Matthew Williams
,
Kendig Sham
,
Serena Belluschi
,
Wenjuan Ma
,
Xiaonan Wang
,
Winnie Lau
,
Kerstin B. Kaufmann
,
Gabriela Krivdova
,
Emily F. Calderbank
,
Nicole Mende
,
Jessica McLeod
,
Giovanna Mantica
,
Juan Li
,
Charlotte Grey-Wilson
,
Michael Drakopoulos
,
Shaaezmeen Basheer
,
Shubhankar Sinha
,
Evangelia Diamanti
,
Christina Basford
,
Nicola K. Wilson
,
Steven J. Howe
,
John E. Dick
,
Berthold Göttgens
,
Anthony R. Green
,
Natalie Francis
,
Elisa Laurenti
·
YOU?
·
· 2024
· Open Access
·
· DOI: https://doi.org/10.1182/blood.2023021426
YOU?
·
· 2024
· Open Access
·
· DOI: https://doi.org/10.1182/blood.2023021426
Loss of long-term hematopoietic stem cell (LT-HSC) function ex vivo hampers the success of clinical protocols that rely on culture. However, the kinetics and mechanisms through which this occurs remain incompletely characterized. In this study, through time-resolved single-cell RNA sequencing, matched in vivo functional analysis, and the use of a reversible in vitro system of early G1 arrest, we defined the sequence of transcriptional and functional events that occur during the first ex vivo division of human LT-HSCs. We demonstrated that the sharpest loss in LT-HSC repopulation capacity happens early on, between 6 and 24 hours of culture, before LT-HSCs commit to cell cycle progression. During this time window, LT-HSCs adapt to the culture environment, limit the global variability in gene expression, and transiently upregulate gene networks involved in signaling and stress responses. From 24 hours, LT-HSC progression past early G1 contributes to the establishment of differentiation programs in culture. However, contrary to the current assumptions, we demonstrated that the loss of HSC function ex vivo is independent of cell cycle progression. Finally, we showed that targeting LT-HSC adaptation to culture by inhibiting the early activation of JAK/STAT signaling improves HSC long-term repopulating function ex vivo. Collectively, our study demonstrated that controlling early LT-HSC adaptation to ex vivo culture, for example, via JAK inhibition, is critically important to improve HSC gene therapy and expansion protocols.
Related Topics
Concepts
Ex vivo
Biology
Haematopoiesis
Stem cell
Cell biology
Hematopoietic stem cell
Cell cycle
Cancer research
Immunology
In vivo
Cell
Genetics
Metadata
- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.1182/blood.2023021426
- OA Status
- hybrid
- Cited By
- 17
- References
- 87
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W4399072471
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
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https://openalex.org/W4399072471Canonical identifier for this work in OpenAlex
- DOI
-
https://doi.org/10.1182/blood.2023021426Digital Object Identifier
- Title
-
Adaptation to ex vivo culture reduces human hematopoietic stem cell activity independently of the cell cycleWork title
- Type
-
articleOpenAlex work type
- Language
-
enPrimary language
- Publication year
-
2024Year of publication
- Publication date
-
2024-05-28Full publication date if available
- Authors
-
Carys Johnson, Matthew Williams, Kendig Sham, Serena Belluschi, Wenjuan Ma, Xiaonan Wang, Winnie Lau, Kerstin B. Kaufmann, Gabriela Krivdova, Emily F. Calderbank, Nicole Mende, Jessica McLeod, Giovanna Mantica, Juan Li, Charlotte Grey-Wilson, Michael Drakopoulos, Shaaezmeen Basheer, Shubhankar Sinha, Evangelia Diamanti, Christina Basford, Nicola K. Wilson, Steven J. Howe, John E. Dick, Berthold Göttgens, Anthony R. Green, Natalie Francis, Elisa LaurentiList of authors in order
- Landing page
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https://doi.org/10.1182/blood.2023021426Publisher landing page
- Open access
-
YesWhether a free full text is available
- OA status
-
hybridOpen access status per OpenAlex
- OA URL
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https://doi.org/10.1182/blood.2023021426Direct OA link when available
- Concepts
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Ex vivo, Biology, Haematopoiesis, Stem cell, Cell biology, Hematopoietic stem cell, Cell cycle, Cancer research, Immunology, In vivo, Cell, GeneticsTop concepts (fields/topics) attached by OpenAlex
- Cited by
-
17Total citation count in OpenAlex
- Citations by year (recent)
-
2025: 11, 2024: 4, 2023: 2Per-year citation counts (last 5 years)
- References (count)
-
87Number of works referenced by this work
- Related works (count)
-
10Other works algorithmically related by OpenAlex
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| abstract_inverted_index.6 | 93 |
| abstract_inverted_index.a | 50 |
| abstract_inverted_index.24 | 95, 135 |
| abstract_inverted_index.G1 | 57, 141 |
| abstract_inverted_index.In | 33 |
| abstract_inverted_index.We | 79 |
| abstract_inverted_index.by | 182 |
| abstract_inverted_index.ex | 9, 73, 165, 195, 207 |
| abstract_inverted_index.in | 42, 52, 85, 120, 129, 149 |
| abstract_inverted_index.is | 167, 215 |
| abstract_inverted_index.of | 2, 14, 49, 55, 63, 76, 97, 146, 162, 169, 187 |
| abstract_inverted_index.on | 19 |
| abstract_inverted_index.to | 102, 112, 143, 153, 180, 206, 218 |
| abstract_inverted_index.we | 59, 157, 174 |
| abstract_inverted_index.HSC | 163, 191, 220 |
| abstract_inverted_index.JAK | 213 |
| abstract_inverted_index.RNA | 39 |
| abstract_inverted_index.and | 24, 46, 65, 94, 123, 131, 223 |
| abstract_inverted_index.for | 210 |
| abstract_inverted_index.on, | 91 |
| abstract_inverted_index.our | 198 |
| abstract_inverted_index.the | 12, 22, 47, 61, 71, 82, 113, 117, 144, 154, 160, 184 |
| abstract_inverted_index.use | 48 |
| abstract_inverted_index.via | 212 |
| abstract_inverted_index.From | 134 |
| abstract_inverted_index.Loss | 1 |
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| abstract_inverted_index.gene | 121, 126, 221 |
| abstract_inverted_index.loss | 84, 161 |
| abstract_inverted_index.past | 139 |
| abstract_inverted_index.rely | 18 |
| abstract_inverted_index.stem | 5 |
| abstract_inverted_index.that | 17, 68, 81, 159, 176, 201 |
| abstract_inverted_index.this | 28, 34, 107 |
| abstract_inverted_index.time | 108 |
| abstract_inverted_index.vivo | 10, 43, 74, 166, 208 |
| abstract_inverted_index.adapt | 111 |
| abstract_inverted_index.cycle | 104, 171 |
| abstract_inverted_index.early | 56, 90, 140, 185, 203 |
| abstract_inverted_index.first | 72 |
| abstract_inverted_index.hours | 96 |
| abstract_inverted_index.human | 77 |
| abstract_inverted_index.limit | 116 |
| abstract_inverted_index.occur | 69 |
| abstract_inverted_index.study | 199 |
| abstract_inverted_index.vitro | 53 |
| abstract_inverted_index.vivo. | 196 |
| abstract_inverted_index.which | 27 |
| abstract_inverted_index.During | 106 |
| abstract_inverted_index.LT-HSC | 86, 137, 178, 204 |
| abstract_inverted_index.before | 99 |
| abstract_inverted_index.commit | 101 |
| abstract_inverted_index.during | 70 |
| abstract_inverted_index.events | 67 |
| abstract_inverted_index.global | 118 |
| abstract_inverted_index.hours, | 136 |
| abstract_inverted_index.occurs | 29 |
| abstract_inverted_index.remain | 30 |
| abstract_inverted_index.showed | 175 |
| abstract_inverted_index.stress | 132 |
| abstract_inverted_index.study, | 35 |
| abstract_inverted_index.system | 54 |
| abstract_inverted_index.LT-HSCs | 100, 110 |
| abstract_inverted_index.arrest, | 58 |
| abstract_inverted_index.between | 92 |
| abstract_inverted_index.culture | 114, 181 |
| abstract_inverted_index.current | 155 |
| abstract_inverted_index.defined | 60 |
| abstract_inverted_index.hampers | 11 |
| abstract_inverted_index.happens | 89 |
| abstract_inverted_index.improve | 219 |
| abstract_inverted_index.matched | 41 |
| abstract_inverted_index.success | 13 |
| abstract_inverted_index.therapy | 222 |
| abstract_inverted_index.through | 26, 36 |
| abstract_inverted_index.window, | 109 |
| abstract_inverted_index.(LT-HSC) | 7 |
| abstract_inverted_index.Abstract | 0 |
| abstract_inverted_index.Finally, | 173 |
| abstract_inverted_index.However, | 21, 151 |
| abstract_inverted_index.JAK/STAT | 188 |
| abstract_inverted_index.LT-HSCs. | 78 |
| abstract_inverted_index.capacity | 88 |
| abstract_inverted_index.clinical | 15 |
| abstract_inverted_index.contrary | 152 |
| abstract_inverted_index.culture, | 98, 209 |
| abstract_inverted_index.culture. | 20, 150 |
| abstract_inverted_index.division | 75 |
| abstract_inverted_index.example, | 211 |
| abstract_inverted_index.function | 8, 164, 194 |
| abstract_inverted_index.improves | 190 |
| abstract_inverted_index.involved | 128 |
| abstract_inverted_index.kinetics | 23 |
| abstract_inverted_index.networks | 127 |
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| abstract_inverted_index.sharpest | 83 |
| abstract_inverted_index.analysis, | 45 |
| abstract_inverted_index.expansion | 224 |
| abstract_inverted_index.important | 217 |
| abstract_inverted_index.long-term | 3, 192 |
| abstract_inverted_index.protocols | 16 |
| abstract_inverted_index.signaling | 130, 189 |
| abstract_inverted_index.targeting | 177 |
| abstract_inverted_index.activation | 186 |
| abstract_inverted_index.adaptation | 179, 205 |
| abstract_inverted_index.critically | 216 |
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| abstract_inverted_index.sequencing, | 40 |
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| abstract_inverted_index.repopulation | 87 |
| abstract_inverted_index.Collectively, | 197 |
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| abstract_inverted_index.hematopoietic | 4 |
| abstract_inverted_index.time-resolved | 37 |
| abstract_inverted_index.characterized. | 32 |
| abstract_inverted_index.differentiation | 147 |
| abstract_inverted_index.transcriptional | 64 |
| cited_by_percentile_year.max | 99 |
| cited_by_percentile_year.min | 94 |
| countries_distinct_count | 2 |
| institutions_distinct_count | 27 |
| citation_normalized_percentile.value | 0.98198556 |
| citation_normalized_percentile.is_in_top_1_percent | True |
| citation_normalized_percentile.is_in_top_10_percent | True |