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A single-cell and single-nucleus RNA-Seq toolbox for fresh and frozen human tumors

Single-cell genomics is essential to chart tumor ecosystems. Although single-cell RNA-Seq (scRNA-Seq) profiles RNA from cells dissociated from fresh tumors, single-nucleus RNA-Seq (snRNA-Seq) is needed to profile frozen or hard-to-dissociate tumors. Each requires customization to different tissue an... Full description

Journal Title: Nature medicine 2020, Vol.26 (5), p.792-802
Main Author: Slyper, Michal
Other Authors: Porter, Caroline B M , Ashenberg, Orr , Waldman, Julia , Drokhlyansky, Eugene , Wakiro, Isaac , Smillie, Christopher , Smith-Rosario, Gabriela , Wu, Jingyi , Dionne, Danielle , Vigneau, Sébastien , Jané-Valbuena, Judit , Tickle, Timothy L , Napolitano, Sara , Su, Mei-Ju , Patel, Anand G , Karlstrom, Asa , Gritsch, Simon , Nomura, Masashi , Waghray, Avinash , Gohil, Satyen H , Tsankov, Alexander M , Jerby-Arnon, Livnat , Cohen, Ofir , Klughammer, Johanna , Rosen, Yanay , Gould, Joshua , Nguyen, Lan , Hofree, Matan , Tramontozzi, Peter J , Li, Bo , Wu, Catherine J , Izar, Benjamin , Haq, Rizwan , Hodi, F Stephen , Yoon, Charles H , Hata, Aaron N , Baker, Suzanne J , Suvà, Mario L , Bueno, Raphael , Stover, Elizabeth H , Clay, Michael R , Dyer, Michael A , Collins, Natalie B , Matulonis, Ursula A , Wagle, Nikhil , Johnson, Bruce E , Rotem, Asaf , Rozenblatt-Rosen, Orit , Regev, Aviv
Format: Electronic Article Electronic Article
Language: English
Subjects:
Publisher: United States: Nature Publishing Group
ID: ISSN: 1078-8956
Link: https://www.ncbi.nlm.nih.gov/pubmed/32405060
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title: A single-cell and single-nucleus RNA-Seq toolbox for fresh and frozen human tumors
format: Article
creator:
  • Slyper, Michal
  • Porter, Caroline B M
  • Ashenberg, Orr
  • Waldman, Julia
  • Drokhlyansky, Eugene
  • Wakiro, Isaac
  • Smillie, Christopher
  • Smith-Rosario, Gabriela
  • Wu, Jingyi
  • Dionne, Danielle
  • Vigneau, Sébastien
  • Jané-Valbuena, Judit
  • Tickle, Timothy L
  • Napolitano, Sara
  • Su, Mei-Ju
  • Patel, Anand G
  • Karlstrom, Asa
  • Gritsch, Simon
  • Nomura, Masashi
  • Waghray, Avinash
  • Gohil, Satyen H
  • Tsankov, Alexander M
  • Jerby-Arnon, Livnat
  • Cohen, Ofir
  • Klughammer, Johanna
  • Rosen, Yanay
  • Gould, Joshua
  • Nguyen, Lan
  • Hofree, Matan
  • Tramontozzi, Peter J
  • Li, Bo
  • Wu, Catherine J
  • Izar, Benjamin
  • Haq, Rizwan
  • Hodi, F Stephen
  • Yoon, Charles H
  • Hata, Aaron N
  • Baker, Suzanne J
  • Suvà, Mario L
  • Bueno, Raphael
  • Stover, Elizabeth H
  • Clay, Michael R
  • Dyer, Michael A
  • Collins, Natalie B
  • Matulonis, Ursula A
  • Wagle, Nikhil
  • Johnson, Bruce E
  • Rotem, Asaf
  • Rozenblatt-Rosen, Orit
  • Regev, Aviv
subjects:
  • Adult
  • Algorithms
  • Animals
  • Atlases
  • Cell Nucleus - chemistry
  • Cell Nucleus - genetics
  • Cell Nucleus - metabolism
  • Child
  • Computational Biology - methods
  • Female
  • Freezing
  • Gene Expression Profiling - methods
  • Gene Expression Regulation, Neoplastic
  • Genomics - methods
  • Humans
  • Identification and classification
  • Mice
  • Mice, Knockout
  • Mice, Nude
  • Neoplasms - genetics
  • Neoplasms - metabolism
  • Neoplasms - pathology
  • Nuclei
  • Nuclei (cytology)
  • Profiling
  • RNA sequencing
  • RNA-Seq - methods
  • Sequence Analysis, RNA - methods
  • Single-Cell Analysis - methods
  • snRNA
  • Tumor Cells, Cultured
  • Tumors
  • Usage
  • Whole Exome Sequencing - methods
ispartof: Nature medicine, 2020, Vol.26 (5), p.792-802
description: Single-cell genomics is essential to chart tumor ecosystems. Although single-cell RNA-Seq (scRNA-Seq) profiles RNA from cells dissociated from fresh tumors, single-nucleus RNA-Seq (snRNA-Seq) is needed to profile frozen or hard-to-dissociate tumors. Each requires customization to different tissue and tumor types, posing a barrier to adoption. Here, we have developed a systematic toolbox for profiling fresh and frozen clinical tumor samples using scRNA-Seq and snRNA-Seq, respectively. We analyzed 216,490 cells and nuclei from 40 samples across 23 specimens spanning eight tumor types of varying tissue and sample characteristics. We evaluated protocols by cell and nucleus quality, recovery rate and cellular composition. scRNA-Seq and snRNA-Seq from matched samples recovered the same cell types, but at different proportions. Our work provides guidance for studies in a broad range of tumors, including criteria for testing and selecting methods from the toolbox for other tumors, thus paving the way for charting tumor atlases.
language: eng
source:
identifier: ISSN: 1078-8956
fulltext: no_fulltext
issn:
  • 1078-8956
  • 1546-170X
url: Link


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titleA single-cell and single-nucleus RNA-Seq toolbox for fresh and frozen human tumors
creatorSlyper, Michal ; Porter, Caroline B M ; Ashenberg, Orr ; Waldman, Julia ; Drokhlyansky, Eugene ; Wakiro, Isaac ; Smillie, Christopher ; Smith-Rosario, Gabriela ; Wu, Jingyi ; Dionne, Danielle ; Vigneau, Sébastien ; Jané-Valbuena, Judit ; Tickle, Timothy L ; Napolitano, Sara ; Su, Mei-Ju ; Patel, Anand G ; Karlstrom, Asa ; Gritsch, Simon ; Nomura, Masashi ; Waghray, Avinash ; Gohil, Satyen H ; Tsankov, Alexander M ; Jerby-Arnon, Livnat ; Cohen, Ofir ; Klughammer, Johanna ; Rosen, Yanay ; Gould, Joshua ; Nguyen, Lan ; Hofree, Matan ; Tramontozzi, Peter J ; Li, Bo ; Wu, Catherine J ; Izar, Benjamin ; Haq, Rizwan ; Hodi, F Stephen ; Yoon, Charles H ; Hata, Aaron N ; Baker, Suzanne J ; Suvà, Mario L ; Bueno, Raphael ; Stover, Elizabeth H ; Clay, Michael R ; Dyer, Michael A ; Collins, Natalie B ; Matulonis, Ursula A ; Wagle, Nikhil ; Johnson, Bruce E ; Rotem, Asaf ; Rozenblatt-Rosen, Orit ; Regev, Aviv
creatorcontribSlyper, Michal ; Porter, Caroline B M ; Ashenberg, Orr ; Waldman, Julia ; Drokhlyansky, Eugene ; Wakiro, Isaac ; Smillie, Christopher ; Smith-Rosario, Gabriela ; Wu, Jingyi ; Dionne, Danielle ; Vigneau, Sébastien ; Jané-Valbuena, Judit ; Tickle, Timothy L ; Napolitano, Sara ; Su, Mei-Ju ; Patel, Anand G ; Karlstrom, Asa ; Gritsch, Simon ; Nomura, Masashi ; Waghray, Avinash ; Gohil, Satyen H ; Tsankov, Alexander M ; Jerby-Arnon, Livnat ; Cohen, Ofir ; Klughammer, Johanna ; Rosen, Yanay ; Gould, Joshua ; Nguyen, Lan ; Hofree, Matan ; Tramontozzi, Peter J ; Li, Bo ; Wu, Catherine J ; Izar, Benjamin ; Haq, Rizwan ; Hodi, F Stephen ; Yoon, Charles H ; Hata, Aaron N ; Baker, Suzanne J ; Suvà, Mario L ; Bueno, Raphael ; Stover, Elizabeth H ; Clay, Michael R ; Dyer, Michael A ; Collins, Natalie B ; Matulonis, Ursula A ; Wagle, Nikhil ; Johnson, Bruce E ; Rotem, Asaf ; Rozenblatt-Rosen, Orit ; Regev, Aviv
descriptionSingle-cell genomics is essential to chart tumor ecosystems. Although single-cell RNA-Seq (scRNA-Seq) profiles RNA from cells dissociated from fresh tumors, single-nucleus RNA-Seq (snRNA-Seq) is needed to profile frozen or hard-to-dissociate tumors. Each requires customization to different tissue and tumor types, posing a barrier to adoption. Here, we have developed a systematic toolbox for profiling fresh and frozen clinical tumor samples using scRNA-Seq and snRNA-Seq, respectively. We analyzed 216,490 cells and nuclei from 40 samples across 23 specimens spanning eight tumor types of varying tissue and sample characteristics. We evaluated protocols by cell and nucleus quality, recovery rate and cellular composition. scRNA-Seq and snRNA-Seq from matched samples recovered the same cell types, but at different proportions. Our work provides guidance for studies in a broad range of tumors, including criteria for testing and selecting methods from the toolbox for other tumors, thus paving the way for charting tumor atlases.
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languageeng
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subjectAdult ; Algorithms ; Animals ; Atlases ; Cell Nucleus - chemistry ; Cell Nucleus - genetics ; Cell Nucleus - metabolism ; Child ; Computational Biology - methods ; Female ; Freezing ; Gene Expression Profiling - methods ; Gene Expression Regulation, Neoplastic ; Genomics - methods ; Humans ; Identification and classification ; Mice ; Mice, Knockout ; Mice, Nude ; Neoplasms - genetics ; Neoplasms - metabolism ; Neoplasms - pathology ; Nuclei ; Nuclei (cytology) ; Profiling ; RNA sequencing ; RNA-Seq - methods ; Sequence Analysis, RNA - methods ; Single-Cell Analysis - methods ; snRNA ; Tumor Cells, Cultured ; Tumors ; Usage ; Whole Exome Sequencing - methods
ispartofNature medicine, 2020, Vol.26 (5), p.792-802
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8Wu, Jingyi
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10Vigneau, Sébastien
11Jané-Valbuena, Judit
12Tickle, Timothy L
13Napolitano, Sara
14Su, Mei-Ju
15Patel, Anand G
16Karlstrom, Asa
17Gritsch, Simon
18Nomura, Masashi
19Waghray, Avinash
20Gohil, Satyen H
21Tsankov, Alexander M
22Jerby-Arnon, Livnat
23Cohen, Ofir
24Klughammer, Johanna
25Rosen, Yanay
26Gould, Joshua
27Nguyen, Lan
28Hofree, Matan
29Tramontozzi, Peter J
30Li, Bo
31Wu, Catherine J
32Izar, Benjamin
33Haq, Rizwan
34Hodi, F Stephen
35Yoon, Charles H
36Hata, Aaron N
37Baker, Suzanne J
38Suvà, Mario L
39Bueno, Raphael
40Stover, Elizabeth H
41Clay, Michael R
42Dyer, Michael A
43Collins, Natalie B
44Matulonis, Ursula A
45Wagle, Nikhil
46Johnson, Bruce E
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title
0A single-cell and single-nucleus RNA-Seq toolbox for fresh and frozen human tumors
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descriptionSingle-cell genomics is essential to chart tumor ecosystems. Although single-cell RNA-Seq (scRNA-Seq) profiles RNA from cells dissociated from fresh tumors, single-nucleus RNA-Seq (snRNA-Seq) is needed to profile frozen or hard-to-dissociate tumors. Each requires customization to different tissue and tumor types, posing a barrier to adoption. Here, we have developed a systematic toolbox for profiling fresh and frozen clinical tumor samples using scRNA-Seq and snRNA-Seq, respectively. We analyzed 216,490 cells and nuclei from 40 samples across 23 specimens spanning eight tumor types of varying tissue and sample characteristics. We evaluated protocols by cell and nucleus quality, recovery rate and cellular composition. scRNA-Seq and snRNA-Seq from matched samples recovered the same cell types, but at different proportions. Our work provides guidance for studies in a broad range of tumors, including criteria for testing and selecting methods from the toolbox for other tumors, thus paving the way for charting tumor atlases.
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6Cell Nucleus - metabolism
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8Computational Biology - methods
9Female
10Freezing
11Gene Expression Profiling - methods
12Gene Expression Regulation, Neoplastic
13Genomics - methods
14Humans
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18Mice, Nude
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20Neoplasms - metabolism
21Neoplasms - pathology
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24Profiling
25RNA sequencing
26RNA-Seq - methods
27Sequence Analysis, RNA - methods
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31Tumors
32Usage
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12Tickle, Timothy L
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14Su, Mei-Ju
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39Bueno, Raphael
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43Collins, Natalie B
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titleA single-cell and single-nucleus RNA-Seq toolbox for fresh and frozen human tumors
authorSlyper, Michal ; Porter, Caroline B M ; Ashenberg, Orr ; Waldman, Julia ; Drokhlyansky, Eugene ; Wakiro, Isaac ; Smillie, Christopher ; Smith-Rosario, Gabriela ; Wu, Jingyi ; Dionne, Danielle ; Vigneau, Sébastien ; Jané-Valbuena, Judit ; Tickle, Timothy L ; Napolitano, Sara ; Su, Mei-Ju ; Patel, Anand G ; Karlstrom, Asa ; Gritsch, Simon ; Nomura, Masashi ; Waghray, Avinash ; Gohil, Satyen H ; Tsankov, Alexander M ; Jerby-Arnon, Livnat ; Cohen, Ofir ; Klughammer, Johanna ; Rosen, Yanay ; Gould, Joshua ; Nguyen, Lan ; Hofree, Matan ; Tramontozzi, Peter J ; Li, Bo ; Wu, Catherine J ; Izar, Benjamin ; Haq, Rizwan ; Hodi, F Stephen ; Yoon, Charles H ; Hata, Aaron N ; Baker, Suzanne J ; Suvà, Mario L ; Bueno, Raphael ; Stover, Elizabeth H ; Clay, Michael R ; Dyer, Michael A ; Collins, Natalie B ; Matulonis, Ursula A ; Wagle, Nikhil ; Johnson, Bruce E ; Rotem, Asaf ; Rozenblatt-Rosen, Orit ; Regev, Aviv
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1Algorithms
2Animals
3Atlases
4Cell Nucleus - chemistry
5Cell Nucleus - genetics
6Cell Nucleus - metabolism
7Child
8Computational Biology - methods
9Female
10Freezing
11Gene Expression Profiling - methods
12Gene Expression Regulation, Neoplastic
13Genomics - methods
14Humans
15Identification and classification
16Mice
17Mice, Knockout
18Mice, Nude
19Neoplasms - genetics
20Neoplasms - metabolism
21Neoplasms - pathology
22Nuclei
23Nuclei (cytology)
24Profiling
25RNA sequencing
26RNA-Seq - methods
27Sequence Analysis, RNA - methods
28Single-Cell Analysis - methods
29snRNA
30Tumor Cells, Cultured
31Tumors
32Usage
33Whole Exome Sequencing - methods
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1Porter, Caroline B M
2Ashenberg, Orr
3Waldman, Julia
4Drokhlyansky, Eugene
5Wakiro, Isaac
6Smillie, Christopher
7Smith-Rosario, Gabriela
8Wu, Jingyi
9Dionne, Danielle
10Vigneau, Sébastien
11Jané-Valbuena, Judit
12Tickle, Timothy L
13Napolitano, Sara
14Su, Mei-Ju
15Patel, Anand G
16Karlstrom, Asa
17Gritsch, Simon
18Nomura, Masashi
19Waghray, Avinash
20Gohil, Satyen H
21Tsankov, Alexander M
22Jerby-Arnon, Livnat
23Cohen, Ofir
24Klughammer, Johanna
25Rosen, Yanay
26Gould, Joshua
27Nguyen, Lan
28Hofree, Matan
29Tramontozzi, Peter J
30Li, Bo
31Wu, Catherine J
32Izar, Benjamin
33Haq, Rizwan
34Hodi, F Stephen
35Yoon, Charles H
36Hata, Aaron N
37Baker, Suzanne J
38Suvà, Mario L
39Bueno, Raphael
40Stover, Elizabeth H
41Clay, Michael R
42Dyer, Michael A
43Collins, Natalie B
44Matulonis, Ursula A
45Wagle, Nikhil
46Johnson, Bruce E
47Rotem, Asaf
48Rozenblatt-Rosen, Orit
49Regev, Aviv
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28Hofree, Matan
29Tramontozzi, Peter J
30Li, Bo
31Wu, Catherine J
32Izar, Benjamin
33Haq, Rizwan
34Hodi, F Stephen
35Yoon, Charles H
36Hata, Aaron N
37Baker, Suzanne J
38Suvà, Mario L
39Bueno, Raphael
40Stover, Elizabeth H
41Clay, Michael R
42Dyer, Michael A
43Collins, Natalie B
44Matulonis, Ursula A
45Wagle, Nikhil
46Johnson, Bruce E
47Rotem, Asaf
48Rozenblatt-Rosen, Orit
49Regev, Aviv
formatjournal
genrearticle
ristypeJOUR
atitleA single-cell and single-nucleus RNA-Seq toolbox for fresh and frozen human tumors
jtitleNature medicine
addtitleNat Med
date2020-05
risdate2020
volume26
issue5
spage792
epage802
pages792-802
issn1078-8956
eissn1546-170X
abstractSingle-cell genomics is essential to chart tumor ecosystems. Although single-cell RNA-Seq (scRNA-Seq) profiles RNA from cells dissociated from fresh tumors, single-nucleus RNA-Seq (snRNA-Seq) is needed to profile frozen or hard-to-dissociate tumors. Each requires customization to different tissue and tumor types, posing a barrier to adoption. Here, we have developed a systematic toolbox for profiling fresh and frozen clinical tumor samples using scRNA-Seq and snRNA-Seq, respectively. We analyzed 216,490 cells and nuclei from 40 samples across 23 specimens spanning eight tumor types of varying tissue and sample characteristics. We evaluated protocols by cell and nucleus quality, recovery rate and cellular composition. scRNA-Seq and snRNA-Seq from matched samples recovered the same cell types, but at different proportions. Our work provides guidance for studies in a broad range of tumors, including criteria for testing and selecting methods from the toolbox for other tumors, thus paving the way for charting tumor atlases.
copUnited States
pubNature Publishing Group
pmid32405060
doi10.1038/s41591-020-0844-1
tpages11
orcidid
0https://orcid.org/0000-0002-6578-3216
1https://orcid.org/0000-0001-9898-5351
2https://orcid.org/0000-0003-3293-3158
3https://orcid.org/0000-0003-1659-8927
4https://orcid.org/0000-0003-3332-9438
5https://orcid.org/0000-0002-5540-0111
6https://orcid.org/0000-0001-9581-5461
7https://orcid.org/0000-0002-1438-8275
8https://orcid.org/0000-0001-6095-7849
9https://orcid.org/0000-0002-3348-5054
10https://orcid.org/0000-0003-3847-7309
11https://orcid.org/0000-0002-1290-9276
12https://orcid.org/0000-0001-6313-3570
oafree_for_read