From clinical specimens to human cancer preclinical models—a journey the NCI-cell line database—25 years later

James L. Mulshine; Peter Ujhazy; Melissa Antman; Christine M. Burgess; Igor Kuzmin; Paul A. Bunn; Bruce E. Johnson; Jack A. Roth; Harvey I. Pass; Sheila M. Ross; Carolyn R. Aldige; Ignacio I. Wistuba; John D. Minna

doi:10.1002/jcb.29564

From clinical specimens to human cancer preclinical models—a journey the NCI-cell line database—25 years later

James L. Mulshine, Peter Ujhazy, Melissa Antman, Christine M. Burgess, Igor Kuzmin, Paul A. Bunn, Bruce E. Johnson, Jack A. Roth, Harvey I. Pass, Sheila M. Ross, Carolyn R. Aldige, Ignacio I. Wistuba, John D. Minna

Research output: Contribution to journal › Article › peer-review

2 Scopus citations

Abstract

The intramural the National Cancer Institute (NCI) and more recently the University of Texas Southwestern Medical Center with many different collaborators comprised a complex, multi-disciplinary team that collaborated to generated large, comprehensively annotated, cell-line related research resources which includes associated clinical, and molecular characterization data. This material has been shared in an anonymized fashion to accelerate progress in overcoming lung cancer, the leading cause of cancer death across the world. However, this cell line collection also includes a range of other cancers derived from patient-donated specimens that have been remarkably valuable for other types of cancer and disease research. A comprehensive analysis conducted by the NCI Center for Research Strategy of the 278 cell lines reported in the original Journal of Cellular Biochemistry Supplement, documents that these cell lines and related products have since been used in more than 14 000 grants, and 33 207 published scientific reports. This has resulted in over 1.2 million citations using at least one cell line. Many publications involve the use of more than one cell line, to understand the value of the resource collectively rather than individually; this method has resulted in 2.9 million citations. In addition, these cell lines have been linked to 422 clinical trials and cited by 4700 patents through publications. For lung cancer alone, the cell lines have been used in the research cited in the development of over 70 National Comprehensive Cancer Network clinical guidelines. Finally, it must be underscored again, that patient altruism enabled the availability of this invaluable research resource.

Original language	English (US)
Pages (from-to)	3986-3999
Number of pages	14
Journal	Journal of Cellular Biochemistry
Volume	121
Issue number	8-9
DOIs	https://doi.org/10.1002/jcb.29564
State	Published - Aug 1 2020

Keywords

adult T-cell Leukemia-lymphoma
cell lines
human cancer preclinical models
lung cancer
mesothelioma
patient donated specimens
precision medicine

ASJC Scopus subject areas

Biochemistry
Molecular Biology
Cell Biology

Access to Document

10.1002/jcb.29564

Cite this

Mulshine, J. L., Ujhazy, P., Antman, M., Burgess, C. M., Kuzmin, I., Bunn, P. A., Johnson, B. E., Roth, J. A., Pass, H. I., Ross, S. M., Aldige, C. R., Wistuba, I. I., & Minna, J. D. (2020). From clinical specimens to human cancer preclinical models—a journey the NCI-cell line database—25 years later. Journal of Cellular Biochemistry, 121(8-9), 3986-3999. https://doi.org/10.1002/jcb.29564

From clinical specimens to human cancer preclinical models—a journey the NCI-cell line database—25 years later. / Mulshine, James L.; Ujhazy, Peter; Antman, Melissa; Burgess, Christine M.; Kuzmin, Igor; Bunn, Paul A.; Johnson, Bruce E.; Roth, Jack A.; Pass, Harvey I.; Ross, Sheila M.; Aldige, Carolyn R.; Wistuba, Ignacio I.; Minna, John D.

In: Journal of Cellular Biochemistry, Vol. 121, No. 8-9, 01.08.2020, p. 3986-3999.

Research output: Contribution to journal › Article › peer-review

Mulshine, JL, Ujhazy, P, Antman, M, Burgess, CM, Kuzmin, I, Bunn, PA, Johnson, BE, Roth, JA, Pass, HI, Ross, SM, Aldige, CR, Wistuba, II & Minna, JD 2020, 'From clinical specimens to human cancer preclinical models—a journey the NCI-cell line database—25 years later', Journal of Cellular Biochemistry, vol. 121, no. 8-9, pp. 3986-3999. https://doi.org/10.1002/jcb.29564

Mulshine, James L. ; Ujhazy, Peter ; Antman, Melissa ; Burgess, Christine M. ; Kuzmin, Igor ; Bunn, Paul A. ; Johnson, Bruce E. ; Roth, Jack A. ; Pass, Harvey I. ; Ross, Sheila M. ; Aldige, Carolyn R. ; Wistuba, Ignacio I. ; Minna, John D. / From clinical specimens to human cancer preclinical models—a journey the NCI-cell line database—25 years later. In: Journal of Cellular Biochemistry. 2020 ; Vol. 121, No. 8-9. pp. 3986-3999.

@article{e543d00e3adc422d8b82b165f91e2d3b,

title = "From clinical specimens to human cancer preclinical models—a journey the NCI-cell line database—25 years later",

abstract = "The intramural the National Cancer Institute (NCI) and more recently the University of Texas Southwestern Medical Center with many different collaborators comprised a complex, multi-disciplinary team that collaborated to generated large, comprehensively annotated, cell-line related research resources which includes associated clinical, and molecular characterization data. This material has been shared in an anonymized fashion to accelerate progress in overcoming lung cancer, the leading cause of cancer death across the world. However, this cell line collection also includes a range of other cancers derived from patient-donated specimens that have been remarkably valuable for other types of cancer and disease research. A comprehensive analysis conducted by the NCI Center for Research Strategy of the 278 cell lines reported in the original Journal of Cellular Biochemistry Supplement, documents that these cell lines and related products have since been used in more than 14 000 grants, and 33 207 published scientific reports. This has resulted in over 1.2 million citations using at least one cell line. Many publications involve the use of more than one cell line, to understand the value of the resource collectively rather than individually; this method has resulted in 2.9 million citations. In addition, these cell lines have been linked to 422 clinical trials and cited by 4700 patents through publications. For lung cancer alone, the cell lines have been used in the research cited in the development of over 70 National Comprehensive Cancer Network clinical guidelines. Finally, it must be underscored again, that patient altruism enabled the availability of this invaluable research resource.",

keywords = "adult T-cell Leukemia-lymphoma, cell lines, human cancer preclinical models, lung cancer, mesothelioma, patient donated specimens, precision medicine",

author = "Mulshine, {James L.} and Peter Ujhazy and Melissa Antman and Burgess, {Christine M.} and Igor Kuzmin and Bunn, {Paul A.} and Johnson, {Bruce E.} and Roth, {Jack A.} and Pass, {Harvey I.} and Ross, {Sheila M.} and Aldige, {Carolyn R.} and Wistuba, {Ignacio I.} and Minna, {John D.}",

note = "Funding Information: More recently, the SPORE has focused on development of patient‐derived xenografts (PDXs) in efforts led by Dr. Jack Roth and which also involved a UTSW collaboration with Drs. Stephen Lam and Yuzhuo Wang of the BC Cancer Research Centre in Canada. In this effort first funded by the SPORE and subsequently by an NCI U54 PDX consortium grant, lung tumor samples were taken directly from patients and implanted in immune‐deficient mice which allowed the growth of human tumor cells. Currently, there are more than 200 such lung cancer PDXs are undergoing molecular characterization, and several of them have been used to generate cell lines. The PDXs and lung cancer cell lines as preclinical models are critical to ongoing drug development and validation studies. In 1991, John Minna and Adi Gazdar moved from the NCI to the University of Texas Southwestern (UTSW) taking the cell line collection with them. There they joined forces with the UT MD Anderson Cancer Center (MDACC) team led by Jack Roth and secured an NCI Specialized Center of Research Excellence (SPORE) grant in lung cancer. This large NCI‐driven translational program gave new opportunities for collaborations with other Lung Cancer SPOREs and lung cancer investigators in the USA and abroad. The tumor cell line repository became a central part of the SPORE Pathology Core which was co‐led by Dr. Gazdar at UTSW and Dr. Ignacio Wistuba at MDACC. The further molecular characterization of the tumor lines as part of the SPORE and their use resulted, for example, in seminal discoveries of the mutational landscape in lung cancer that would drive the development of targeted therapies representing a new era in lung cancer treatment. 2.4 Funding Information: We gratefully acknowledge the essential contribution of the patients, trainees, staff and administration at the Washington DC VA, National Naval Medical Center, National Institute of Health Clinical Center, Texas Southwest, M. D. Anderson Cancer Center, and Dana Farber Cancer Center who supported the research described in this manuscript. In particular, we acknowledge the contributions of all of the surgeons, fellows and house officers who contributed to this effort at the VA, Naval Hospital, Bethesda and the NCI with special thanks to Dr. Bimal C. Ghosh's efforts as they collectively ensured that the appropriate biopsy or cytological specimens were obtained and transported to allow the research activity to proceed. We further acknowledge the gracious work of the research nurses and data scientists, who are also critical unsung heroes in enabling such comprehensive research to proceed. We also acknowledge the central contribution of the late Adi F. Gazdar in spearheading the cell line generation efforts. We note that critical and significant contributions of the many international researchers who were deeply engaged in every aspect of this work. We also acknowledge the work of the American Type Culture Collection in their efforts in distributing and curating these valuable cellular reagents. We thank Dr. Toby Hecht for her critical review of the manuscript. We acknowledge the core of virtually all of the work discussed in this manuscript involved federal funding with most provided by the National Institutes of Health and especially the National Cancer Institute. Finally, we again acknowledge the generosity and altruism of the patients whose donated tissue made all this work possible and whose indomitable spirit motivated so many health professionals to remain engaged in this challenging area to ensure that progress did in fact occur. Funding Information: We gratefully acknowledge the essential contribution of the patients, trainees, staff and administration at the Washington DC VA, National Naval Medical Center, National Institute of Health Clinical Center, Texas Southwest, M. D. Anderson Cancer Center, and Dana Farber Cancer Center who supported the research described in this manuscript. In particular, we acknowledge the contributions of all of the surgeons, fellows and house officers who contributed to this effort at the VA, Naval Hospital, Bethesda and the NCI with special thanks to Dr. Bimal C. Ghosh's efforts as they collectively ensured that the appropriate biopsy or cytological specimens were obtained and transported to allow the research activity to proceed. We further acknowledge the gracious work of the research nurses and data scientists, who are also critical unsung heroes in enabling such comprehensive research to proceed. We also acknowledge the central contribution of the late Adi F. Gazdar in spearheading the cell line generation efforts. We note that critical and significant contributions of the many international researchers who were deeply engaged in every aspect of this work. We also acknowledge the work of the American Type Culture Collection in their efforts in distributing and curating these valuable cellular reagents. We thank Dr. Toby Hecht for her critical review of the manuscript. We acknowledge the core of virtually all of the work discussed in this manuscript involved federal funding with most provided by the National Institutes of Health and especially the National Cancer Institute. Finally, we again acknowledge the generosity and altruism of the patients whose donated tissue made all this work possible and whose indomitable spirit motivated so many health professionals to remain engaged in this challenging area to ensure that progress did in fact occur. Funding Information: Christine Burgess: I have the following conflicts as related to below with management plan. I am currently employed by Digital Science, the maker of the Dimensions publication database utilized in the analysis; Bruce Johnson: I receive post‐marketing royalties from Dana‐Farber for EGFR mutation testing Paid Consultant for Novartis, Hengrui Therapeutics, and Foundation Medicine Steering Committee for Novartis and Array Biopharma Research Support from Novartis and Cannon Imaging; John D. Minna: Has received cell line licensing royalties from the NCI and cell line licensing royalties from the University of Texas Southwestern Medical Center; Jack A. Roth: Consultant, stock owner (including pending patents) in Genprex, Inc.; Harvey I. Pass: Dr. Pass receives royalties from the NCI for the licensing of cell lines described in this manuscript; Ignacio Wistuba: Advisory Board: Genentech/Roche, Bayer, Bristol‐Myers Squibb, Astra Zeneca/Medimmune, Pfizer, HTG Molecular, Asuragen, Merck, GlaxoSmithKline, Guardant Health and MSD. Speaker: Medscape, MSD, Genentech/Roche, Pfizer. Research support: Genentech, Oncoplex, HTG Molecular, DepArray, Merck, Bristol‐Myers Squibb, Medimmune, Adaptive, Adaptimmune, EMD Serono, Pfizer, Takeda, Amgen, Karus, Johnson & Johnson, Bayer, Iovance, 4D, Novartis, and Akoya. Publisher Copyright: {\textcopyright} 2019 The Authors. Journal of Cellular Biochemistry published by Wiley-VCH Verlag GmbH & Co. KGaA",

year = "2020",

month = aug,

day = "1",

doi = "10.1002/jcb.29564",

language = "English (US)",

volume = "121",

pages = "3986--3999",

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TY - JOUR

T1 - From clinical specimens to human cancer preclinical models—a journey the NCI-cell line database—25 years later

AU - Mulshine, James L.

AU - Ujhazy, Peter

AU - Antman, Melissa

AU - Burgess, Christine M.

AU - Kuzmin, Igor

AU - Bunn, Paul A.

AU - Johnson, Bruce E.

AU - Roth, Jack A.

AU - Pass, Harvey I.

AU - Ross, Sheila M.

AU - Aldige, Carolyn R.

AU - Wistuba, Ignacio I.

AU - Minna, John D.

N1 - Funding Information: More recently, the SPORE has focused on development of patient‐derived xenografts (PDXs) in efforts led by Dr. Jack Roth and which also involved a UTSW collaboration with Drs. Stephen Lam and Yuzhuo Wang of the BC Cancer Research Centre in Canada. In this effort first funded by the SPORE and subsequently by an NCI U54 PDX consortium grant, lung tumor samples were taken directly from patients and implanted in immune‐deficient mice which allowed the growth of human tumor cells. Currently, there are more than 200 such lung cancer PDXs are undergoing molecular characterization, and several of them have been used to generate cell lines. The PDXs and lung cancer cell lines as preclinical models are critical to ongoing drug development and validation studies. In 1991, John Minna and Adi Gazdar moved from the NCI to the University of Texas Southwestern (UTSW) taking the cell line collection with them. There they joined forces with the UT MD Anderson Cancer Center (MDACC) team led by Jack Roth and secured an NCI Specialized Center of Research Excellence (SPORE) grant in lung cancer. This large NCI‐driven translational program gave new opportunities for collaborations with other Lung Cancer SPOREs and lung cancer investigators in the USA and abroad. The tumor cell line repository became a central part of the SPORE Pathology Core which was co‐led by Dr. Gazdar at UTSW and Dr. Ignacio Wistuba at MDACC. The further molecular characterization of the tumor lines as part of the SPORE and their use resulted, for example, in seminal discoveries of the mutational landscape in lung cancer that would drive the development of targeted therapies representing a new era in lung cancer treatment. 2.4 Funding Information: We gratefully acknowledge the essential contribution of the patients, trainees, staff and administration at the Washington DC VA, National Naval Medical Center, National Institute of Health Clinical Center, Texas Southwest, M. D. Anderson Cancer Center, and Dana Farber Cancer Center who supported the research described in this manuscript. In particular, we acknowledge the contributions of all of the surgeons, fellows and house officers who contributed to this effort at the VA, Naval Hospital, Bethesda and the NCI with special thanks to Dr. Bimal C. Ghosh's efforts as they collectively ensured that the appropriate biopsy or cytological specimens were obtained and transported to allow the research activity to proceed. We further acknowledge the gracious work of the research nurses and data scientists, who are also critical unsung heroes in enabling such comprehensive research to proceed. We also acknowledge the central contribution of the late Adi F. Gazdar in spearheading the cell line generation efforts. We note that critical and significant contributions of the many international researchers who were deeply engaged in every aspect of this work. We also acknowledge the work of the American Type Culture Collection in their efforts in distributing and curating these valuable cellular reagents. We thank Dr. Toby Hecht for her critical review of the manuscript. We acknowledge the core of virtually all of the work discussed in this manuscript involved federal funding with most provided by the National Institutes of Health and especially the National Cancer Institute. Finally, we again acknowledge the generosity and altruism of the patients whose donated tissue made all this work possible and whose indomitable spirit motivated so many health professionals to remain engaged in this challenging area to ensure that progress did in fact occur. Funding Information: We gratefully acknowledge the essential contribution of the patients, trainees, staff and administration at the Washington DC VA, National Naval Medical Center, National Institute of Health Clinical Center, Texas Southwest, M. D. Anderson Cancer Center, and Dana Farber Cancer Center who supported the research described in this manuscript. In particular, we acknowledge the contributions of all of the surgeons, fellows and house officers who contributed to this effort at the VA, Naval Hospital, Bethesda and the NCI with special thanks to Dr. Bimal C. Ghosh's efforts as they collectively ensured that the appropriate biopsy or cytological specimens were obtained and transported to allow the research activity to proceed. We further acknowledge the gracious work of the research nurses and data scientists, who are also critical unsung heroes in enabling such comprehensive research to proceed. We also acknowledge the central contribution of the late Adi F. Gazdar in spearheading the cell line generation efforts. We note that critical and significant contributions of the many international researchers who were deeply engaged in every aspect of this work. We also acknowledge the work of the American Type Culture Collection in their efforts in distributing and curating these valuable cellular reagents. We thank Dr. Toby Hecht for her critical review of the manuscript. We acknowledge the core of virtually all of the work discussed in this manuscript involved federal funding with most provided by the National Institutes of Health and especially the National Cancer Institute. Finally, we again acknowledge the generosity and altruism of the patients whose donated tissue made all this work possible and whose indomitable spirit motivated so many health professionals to remain engaged in this challenging area to ensure that progress did in fact occur. Funding Information: Christine Burgess: I have the following conflicts as related to below with management plan. I am currently employed by Digital Science, the maker of the Dimensions publication database utilized in the analysis; Bruce Johnson: I receive post‐marketing royalties from Dana‐Farber for EGFR mutation testing Paid Consultant for Novartis, Hengrui Therapeutics, and Foundation Medicine Steering Committee for Novartis and Array Biopharma Research Support from Novartis and Cannon Imaging; John D. Minna: Has received cell line licensing royalties from the NCI and cell line licensing royalties from the University of Texas Southwestern Medical Center; Jack A. Roth: Consultant, stock owner (including pending patents) in Genprex, Inc.; Harvey I. Pass: Dr. Pass receives royalties from the NCI for the licensing of cell lines described in this manuscript; Ignacio Wistuba: Advisory Board: Genentech/Roche, Bayer, Bristol‐Myers Squibb, Astra Zeneca/Medimmune, Pfizer, HTG Molecular, Asuragen, Merck, GlaxoSmithKline, Guardant Health and MSD. Speaker: Medscape, MSD, Genentech/Roche, Pfizer. Research support: Genentech, Oncoplex, HTG Molecular, DepArray, Merck, Bristol‐Myers Squibb, Medimmune, Adaptive, Adaptimmune, EMD Serono, Pfizer, Takeda, Amgen, Karus, Johnson & Johnson, Bayer, Iovance, 4D, Novartis, and Akoya. Publisher Copyright: © 2019 The Authors. Journal of Cellular Biochemistry published by Wiley-VCH Verlag GmbH & Co. KGaA

PY - 2020/8/1

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N2 - The intramural the National Cancer Institute (NCI) and more recently the University of Texas Southwestern Medical Center with many different collaborators comprised a complex, multi-disciplinary team that collaborated to generated large, comprehensively annotated, cell-line related research resources which includes associated clinical, and molecular characterization data. This material has been shared in an anonymized fashion to accelerate progress in overcoming lung cancer, the leading cause of cancer death across the world. However, this cell line collection also includes a range of other cancers derived from patient-donated specimens that have been remarkably valuable for other types of cancer and disease research. A comprehensive analysis conducted by the NCI Center for Research Strategy of the 278 cell lines reported in the original Journal of Cellular Biochemistry Supplement, documents that these cell lines and related products have since been used in more than 14 000 grants, and 33 207 published scientific reports. This has resulted in over 1.2 million citations using at least one cell line. Many publications involve the use of more than one cell line, to understand the value of the resource collectively rather than individually; this method has resulted in 2.9 million citations. In addition, these cell lines have been linked to 422 clinical trials and cited by 4700 patents through publications. For lung cancer alone, the cell lines have been used in the research cited in the development of over 70 National Comprehensive Cancer Network clinical guidelines. Finally, it must be underscored again, that patient altruism enabled the availability of this invaluable research resource.

AB - The intramural the National Cancer Institute (NCI) and more recently the University of Texas Southwestern Medical Center with many different collaborators comprised a complex, multi-disciplinary team that collaborated to generated large, comprehensively annotated, cell-line related research resources which includes associated clinical, and molecular characterization data. This material has been shared in an anonymized fashion to accelerate progress in overcoming lung cancer, the leading cause of cancer death across the world. However, this cell line collection also includes a range of other cancers derived from patient-donated specimens that have been remarkably valuable for other types of cancer and disease research. A comprehensive analysis conducted by the NCI Center for Research Strategy of the 278 cell lines reported in the original Journal of Cellular Biochemistry Supplement, documents that these cell lines and related products have since been used in more than 14 000 grants, and 33 207 published scientific reports. This has resulted in over 1.2 million citations using at least one cell line. Many publications involve the use of more than one cell line, to understand the value of the resource collectively rather than individually; this method has resulted in 2.9 million citations. In addition, these cell lines have been linked to 422 clinical trials and cited by 4700 patents through publications. For lung cancer alone, the cell lines have been used in the research cited in the development of over 70 National Comprehensive Cancer Network clinical guidelines. Finally, it must be underscored again, that patient altruism enabled the availability of this invaluable research resource.

KW - adult T-cell Leukemia-lymphoma

KW - cell lines

KW - human cancer preclinical models

KW - lung cancer

KW - mesothelioma

KW - patient donated specimens

KW - precision medicine

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JO - Journal of supramolecular structure and cellular biochemistry

JF - Journal of supramolecular structure and cellular biochemistry

SN - 0730-2312

IS - 8-9

ER -

From clinical specimens to human cancer preclinical models—a journey the NCI-cell line database—25 years later

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