Spatial mapping of cellular senescence: emerging challenges and opportunities

Aditi U. Gurkar; Akos A. Gerencser; Ana L. Mora; Andrew C. Nelson; Anru R. Zhang; Anthony B. Lagnado; Archibald Enninful; Christopher Benz; David Furman; Delphine Beaulieu; Diana Jurk; Elizabeth L. Thompson; Fei Wu; Fernanda Rodriguez; Grant Barthel; Hao Chen; Hemali Phatnani; Indra Heckenbach; Jeffrey H. Chuang; Jeremy Horrell; Joana Petrescu; Jonathan K. Alder; Jun Hee Lee; Laura J. Niedernhofer; Manoj Kumar; Melanie Königshoff; Marta Bueno; Miiko Sokka; Morten Scheibye-Knudsen; Nicola Neretti; Oliver Eickelberg; Peter D. Adams; Qianjiang Hu; Quan Zhu; Rebecca A. Porritt; Runze Dong; Samuel Peters; Stella Victorelli; Thomas Pengo; Timur Khaliullin; Vidyani Suryadevara; Xiaonan Fu; Ziv Bar-Joseph; Zhicheng Ji; João F. Passos

doi:10.1038/s43587-023-00446-6

Spatial mapping of cellular senescence: emerging challenges and opportunities

Aditi U. Gurkar, Akos A. Gerencser, Ana L. Mora, Andrew C. Nelson, Anru R. Zhang, Anthony B. Lagnado, Archibald Enninful, Christopher Benz, David Furman, Delphine Beaulieu, Diana Jurk, Elizabeth L. Thompson, Fei Wu, Fernanda Rodriguez, Grant Barthel, Hao Chen, Hemali Phatnani, Indra Heckenbach, Jeffrey H. Chuang, Jeremy HorrellJoana Petrescu, Jonathan K. Alder, Jun Hee Lee, Laura J. Niedernhofer, Manoj Kumar, Melanie Königshoff, Marta Bueno, Miiko Sokka, Morten Scheibye-Knudsen, Nicola Neretti, Oliver Eickelberg, Peter D. Adams, Qianjiang Hu, Quan Zhu, Rebecca A. Porritt, Runze Dong, Samuel Peters, Stella Victorelli, Thomas Pengo, Timur Khaliullin, Vidyani Suryadevara, Xiaonan Fu, Ziv Bar-Joseph, Zhicheng Ji, João F. Passos

Research output: Contribution to journal › Review article › peer-review

66 Scopus citations

Abstract

Cellular senescence is a well-established driver of aging and age-related diseases. There are many challenges to mapping senescent cells in tissues such as the absence of specific markers and their relatively low abundance and vast heterogeneity. Single-cell technologies have allowed unprecedented characterization of senescence; however, many methodologies fail to provide spatial insights. The spatial component is essential, as senescent cells communicate with neighboring cells, impacting their function and the composition of extracellular space. The Cellular Senescence Network (SenNet), a National Institutes of Health (NIH) Common Fund initiative, aims to map senescent cells across the lifespan of humans and mice. Here, we provide a comprehensive review of the existing and emerging methodologies for spatial imaging and their application toward mapping senescent cells. Moreover, we discuss the limitations and challenges inherent to each technology. We argue that the development of spatially resolved methods is essential toward the goal of attaining an atlas of senescent cells.

Original language	English (US)
Pages (from-to)	776-790
Number of pages	15
Journal	Nature Aging
Volume	3
Issue number	7
DOIs	https://doi.org/10.1038/s43587-023-00446-6
State	Published - Jul 2023

Bibliographical note

Funding Information:
This research was supported by the NIH Common Fund, through the Office of Strategic Coordination and the Office of the NIH Director under awards UG3CA268103 (J.F.P., A.B.L., S.V., D.J.), U54AG075931 (A.U.G., A.L.M., D.B., H.C., J.K.A., M.B., M. Königshoff., O.E., Q.H., T.K.), UG3CA268202 (N.N.), U54AG075941 (J.H.C.), UG3CA268091 (J.H.L.), UG3CA268096 (R.D., X.F.), U54AG075931 (Z.B.-J.), U24CA268108 (Z.B.-J.), U54AG076041 (L.J.N., A.C.N., E.L.T., S.P., F.R., G.B.), U54AG075936 (A.R.Z., Z.J.), U54AG079758 (P.D.A., Q.Z., R.A.P.), U54AG076040 (H.P., J.P.), U54 AG075932 (D.F., A.A.G., C.B., F.W., I.H.), UG3CA268112 (V.S., M. Kumar.). We thank A. Impagliazzo for her work on the illustrations.

Funding Information:
This research was supported by the NIH Common Fund, through the Office of Strategic Coordination and the Office of the NIH Director under awards UG3CA268103 (J.F.P., A.B.L., S.V., D.J.), U54AG075931 (A.U.G., A.L.M., D.B., H.C., J.K.A., M.B., M. Königshoff., O.E., Q.H., T.K.), UG3CA268202 (N.N.), U54AG075941 (J.H.C.), UG3CA268091 (J.H.L.), UG3CA268096 (R.D., X.F.), U54AG075931 (Z.B.-J.), U24CA268108 (Z.B.-J.), U54AG076041 (L.J.N., A.C.N., E.L.T., S.P., F.R., G.B.), U54AG075936 (A.R.Z., Z.J.), U54AG079758 (P.D.A., Q.Z., R.A.P.), U54AG076040 (H.P., J.P.), U54 AG075932 (D.F., A.A.G., C.B., F.W., I.H.), UG3CA268112 (V.S., M. Kumar.). We thank A. Impagliazzo for her work on the illustrations.

Publisher Copyright:
© 2023, Springer Nature America, Inc.

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Gurkar, A. U., Gerencser, A. A., Mora, A. L., Nelson, A. C., Zhang, A. R., Lagnado, A. B., Enninful, A., Benz, C., Furman, D., Beaulieu, D., Jurk, D., Thompson, E. L., Wu, F., Rodriguez, F., Barthel, G., Chen, H., Phatnani, H., Heckenbach, I., Chuang, J. H., ... Passos, J. F. (2023). Spatial mapping of cellular senescence: emerging challenges and opportunities. Nature Aging, 3(7), 776-790. https://doi.org/10.1038/s43587-023-00446-6

Gurkar, AU, Gerencser, AA, Mora, AL, Nelson, AC, Zhang, AR, Lagnado, AB, Enninful, A, Benz, C, Furman, D, Beaulieu, D, Jurk, D, Thompson, EL, Wu, F, Rodriguez, F, Barthel, G, Chen, H, Phatnani, H, Heckenbach, I, Chuang, JH, Horrell, J, Petrescu, J, Alder, JK, Lee, JH, Niedernhofer, LJ, Kumar, M, Königshoff, M, Bueno, M, Sokka, M, Scheibye-Knudsen, M, Neretti, N, Eickelberg, O, Adams, PD, Hu, Q, Zhu, Q, Porritt, RA, Dong, R, Peters, S, Victorelli, S, Pengo, T, Khaliullin, T, Suryadevara, V, Fu, X, Bar-Joseph, Z, Ji, Z & Passos, JF 2023, 'Spatial mapping of cellular senescence: emerging challenges and opportunities', Nature Aging, vol. 3, no. 7, pp. 776-790. https://doi.org/10.1038/s43587-023-00446-6

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title = "Spatial mapping of cellular senescence: emerging challenges and opportunities",

abstract = "Cellular senescence is a well-established driver of aging and age-related diseases. There are many challenges to mapping senescent cells in tissues such as the absence of specific markers and their relatively low abundance and vast heterogeneity. Single-cell technologies have allowed unprecedented characterization of senescence; however, many methodologies fail to provide spatial insights. The spatial component is essential, as senescent cells communicate with neighboring cells, impacting their function and the composition of extracellular space. The Cellular Senescence Network (SenNet), a National Institutes of Health (NIH) Common Fund initiative, aims to map senescent cells across the lifespan of humans and mice. Here, we provide a comprehensive review of the existing and emerging methodologies for spatial imaging and their application toward mapping senescent cells. Moreover, we discuss the limitations and challenges inherent to each technology. We argue that the development of spatially resolved methods is essential toward the goal of attaining an atlas of senescent cells.",

author = "Gurkar, {Aditi U.} and Gerencser, {Akos A.} and Mora, {Ana L.} and Nelson, {Andrew C.} and Zhang, {Anru R.} and Lagnado, {Anthony B.} and Archibald Enninful and Christopher Benz and David Furman and Delphine Beaulieu and Diana Jurk and Thompson, {Elizabeth L.} and Fei Wu and Fernanda Rodriguez and Grant Barthel and Hao Chen and Hemali Phatnani and Indra Heckenbach and Chuang, {Jeffrey H.} and Jeremy Horrell and Joana Petrescu and Alder, {Jonathan K.} and Lee, {Jun Hee} and Niedernhofer, {Laura J.} and Manoj Kumar and Melanie K{\"o}nigshoff and Marta Bueno and Miiko Sokka and Morten Scheibye-Knudsen and Nicola Neretti and Oliver Eickelberg and Adams, {Peter D.} and Qianjiang Hu and Quan Zhu and Porritt, {Rebecca A.} and Runze Dong and Samuel Peters and Stella Victorelli and Thomas Pengo and Timur Khaliullin and Vidyani Suryadevara and Xiaonan Fu and Ziv Bar-Joseph and Zhicheng Ji and Passos, {Jo{\~a}o F.}",

note = "Funding Information: This research was supported by the NIH Common Fund, through the Office of Strategic Coordination and the Office of the NIH Director under awards UG3CA268103 (J.F.P., A.B.L., S.V., D.J.), U54AG075931 (A.U.G., A.L.M., D.B., H.C., J.K.A., M.B., M. K{\"o}nigshoff., O.E., Q.H., T.K.), UG3CA268202 (N.N.), U54AG075941 (J.H.C.), UG3CA268091 (J.H.L.), UG3CA268096 (R.D., X.F.), U54AG075931 (Z.B.-J.), U24CA268108 (Z.B.-J.), U54AG076041 (L.J.N., A.C.N., E.L.T., S.P., F.R., G.B.), U54AG075936 (A.R.Z., Z.J.), U54AG079758 (P.D.A., Q.Z., R.A.P.), U54AG076040 (H.P., J.P.), U54 AG075932 (D.F., A.A.G., C.B., F.W., I.H.), UG3CA268112 (V.S., M. Kumar.). We thank A. Impagliazzo for her work on the illustrations. Funding Information: This research was supported by the NIH Common Fund, through the Office of Strategic Coordination and the Office of the NIH Director under awards UG3CA268103 (J.F.P., A.B.L., S.V., D.J.), U54AG075931 (A.U.G., A.L.M., D.B., H.C., J.K.A., M.B., M. K{\"o}nigshoff., O.E., Q.H., T.K.), UG3CA268202 (N.N.), U54AG075941 (J.H.C.), UG3CA268091 (J.H.L.), UG3CA268096 (R.D., X.F.), U54AG075931 (Z.B.-J.), U24CA268108 (Z.B.-J.), U54AG076041 (L.J.N., A.C.N., E.L.T., S.P., F.R., G.B.), U54AG075936 (A.R.Z., Z.J.), U54AG079758 (P.D.A., Q.Z., R.A.P.), U54AG076040 (H.P., J.P.), U54 AG075932 (D.F., A.A.G., C.B., F.W., I.H.), UG3CA268112 (V.S., M. Kumar.). We thank A. Impagliazzo for her work on the illustrations. Publisher Copyright: {\textcopyright} 2023, Springer Nature America, Inc.",

year = "2023",

month = jul,

doi = "10.1038/s43587-023-00446-6",

language = "English (US)",

volume = "3",

pages = "776--790",

journal = "Nature Aging",

issn = "2662-8465",

publisher = "Springer",

number = "7",

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TY - JOUR

T1 - Spatial mapping of cellular senescence

T2 - emerging challenges and opportunities

AU - Gurkar, Aditi U.

AU - Gerencser, Akos A.

AU - Mora, Ana L.

AU - Nelson, Andrew C.

AU - Zhang, Anru R.

AU - Lagnado, Anthony B.

AU - Enninful, Archibald

AU - Benz, Christopher

AU - Furman, David

AU - Beaulieu, Delphine

AU - Jurk, Diana

AU - Thompson, Elizabeth L.

AU - Wu, Fei

AU - Rodriguez, Fernanda

AU - Barthel, Grant

AU - Chen, Hao

AU - Phatnani, Hemali

AU - Heckenbach, Indra

AU - Chuang, Jeffrey H.

AU - Horrell, Jeremy

AU - Petrescu, Joana

AU - Alder, Jonathan K.

AU - Lee, Jun Hee

AU - Niedernhofer, Laura J.

AU - Kumar, Manoj

AU - Königshoff, Melanie

AU - Bueno, Marta

AU - Sokka, Miiko

AU - Scheibye-Knudsen, Morten

AU - Neretti, Nicola

AU - Eickelberg, Oliver

AU - Adams, Peter D.

AU - Hu, Qianjiang

AU - Zhu, Quan

AU - Porritt, Rebecca A.

AU - Dong, Runze

AU - Peters, Samuel

AU - Victorelli, Stella

AU - Pengo, Thomas

AU - Khaliullin, Timur

AU - Suryadevara, Vidyani

AU - Fu, Xiaonan

AU - Bar-Joseph, Ziv

AU - Ji, Zhicheng

AU - Passos, João F.

N1 - Funding Information: This research was supported by the NIH Common Fund, through the Office of Strategic Coordination and the Office of the NIH Director under awards UG3CA268103 (J.F.P., A.B.L., S.V., D.J.), U54AG075931 (A.U.G., A.L.M., D.B., H.C., J.K.A., M.B., M. Königshoff., O.E., Q.H., T.K.), UG3CA268202 (N.N.), U54AG075941 (J.H.C.), UG3CA268091 (J.H.L.), UG3CA268096 (R.D., X.F.), U54AG075931 (Z.B.-J.), U24CA268108 (Z.B.-J.), U54AG076041 (L.J.N., A.C.N., E.L.T., S.P., F.R., G.B.), U54AG075936 (A.R.Z., Z.J.), U54AG079758 (P.D.A., Q.Z., R.A.P.), U54AG076040 (H.P., J.P.), U54 AG075932 (D.F., A.A.G., C.B., F.W., I.H.), UG3CA268112 (V.S., M. Kumar.). We thank A. Impagliazzo for her work on the illustrations. Funding Information: This research was supported by the NIH Common Fund, through the Office of Strategic Coordination and the Office of the NIH Director under awards UG3CA268103 (J.F.P., A.B.L., S.V., D.J.), U54AG075931 (A.U.G., A.L.M., D.B., H.C., J.K.A., M.B., M. Königshoff., O.E., Q.H., T.K.), UG3CA268202 (N.N.), U54AG075941 (J.H.C.), UG3CA268091 (J.H.L.), UG3CA268096 (R.D., X.F.), U54AG075931 (Z.B.-J.), U24CA268108 (Z.B.-J.), U54AG076041 (L.J.N., A.C.N., E.L.T., S.P., F.R., G.B.), U54AG075936 (A.R.Z., Z.J.), U54AG079758 (P.D.A., Q.Z., R.A.P.), U54AG076040 (H.P., J.P.), U54 AG075932 (D.F., A.A.G., C.B., F.W., I.H.), UG3CA268112 (V.S., M. Kumar.). We thank A. Impagliazzo for her work on the illustrations. Publisher Copyright: © 2023, Springer Nature America, Inc.

PY - 2023/7

Y1 - 2023/7

N2 - Cellular senescence is a well-established driver of aging and age-related diseases. There are many challenges to mapping senescent cells in tissues such as the absence of specific markers and their relatively low abundance and vast heterogeneity. Single-cell technologies have allowed unprecedented characterization of senescence; however, many methodologies fail to provide spatial insights. The spatial component is essential, as senescent cells communicate with neighboring cells, impacting their function and the composition of extracellular space. The Cellular Senescence Network (SenNet), a National Institutes of Health (NIH) Common Fund initiative, aims to map senescent cells across the lifespan of humans and mice. Here, we provide a comprehensive review of the existing and emerging methodologies for spatial imaging and their application toward mapping senescent cells. Moreover, we discuss the limitations and challenges inherent to each technology. We argue that the development of spatially resolved methods is essential toward the goal of attaining an atlas of senescent cells.

AB - Cellular senescence is a well-established driver of aging and age-related diseases. There are many challenges to mapping senescent cells in tissues such as the absence of specific markers and their relatively low abundance and vast heterogeneity. Single-cell technologies have allowed unprecedented characterization of senescence; however, many methodologies fail to provide spatial insights. The spatial component is essential, as senescent cells communicate with neighboring cells, impacting their function and the composition of extracellular space. The Cellular Senescence Network (SenNet), a National Institutes of Health (NIH) Common Fund initiative, aims to map senescent cells across the lifespan of humans and mice. Here, we provide a comprehensive review of the existing and emerging methodologies for spatial imaging and their application toward mapping senescent cells. Moreover, we discuss the limitations and challenges inherent to each technology. We argue that the development of spatially resolved methods is essential toward the goal of attaining an atlas of senescent cells.

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SN - 2662-8465

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EP - 790

JO - Nature Aging

JF - Nature Aging

IS - 7

ER -

Spatial mapping of cellular senescence: emerging challenges and opportunities

Abstract

Bibliographical note

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Spatial mapping of cellular senescence: emerging challenges and opportunities

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