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Article ; Online: Translation of Precision Medicine Research Into Biomarker-Informed Care in Radiation Oncology.

Scarborough, Jessica A / Scott, Jacob G

2021 Volume 32, Issue 1, Page(s) 42–53

Abstract: The reach of personalized medicine in radiation oncology has expanded greatly over the past few decades as technical precision has improved the delivery of radiation to each patient's unique anatomy. Yet, the consideration of biological heterogeneity ... ...

Abstract	The reach of personalized medicine in radiation oncology has expanded greatly over the past few decades as technical precision has improved the delivery of radiation to each patient's unique anatomy. Yet, the consideration of biological heterogeneity between patients has largely not been translated to clinical care. There are innumerable promising advancements in the discovery and validation of biomarkers, which could be used to alter radiation therapy directly or indirectly. Directly, biomarker-informed care may alter treatment dose or identify patients who would benefit most from radiation therapy and who could safely avoid more aggressive care. Indirectly, a variety of biomarkers could assist with choosing the best radiosensitizing chemotherapies. The translation of these advancements into clinical practice will bring radiation oncology even further into the era of precision medicine, treating patients according to their unique anatomical and biological differences.
MeSH term(s)	Biomarkers ; Humans ; Neoplasms/radiotherapy ; Precision Medicine ; Radiation Oncology
Chemical Substances	Biomarkers
Language	English
Publishing date	2021-11-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	1146999-7
ISSN	1532-9461 ; 1053-4296
ISSN (online)	1532-9461
ISSN	1053-4296
DOI	10.1016/j.semradonc.2021.09.001
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Article ; Online: Evolution-Informed Strategies for Combating Drug Resistance in Cancer.

Lin-Rahardja, Kristi / Weaver, Davis T / Scarborough, Jessica A / Scott, Jacob G

International journal of molecular sciences

2023 Volume 24, Issue 7

Abstract: The ever-changing nature of cancer poses the most difficult challenge oncologists face today. Cancer's remarkable adaptability has inspired many to work toward understanding the evolutionary dynamics that underlie this disease in hopes of learning new ... ...

Abstract	The ever-changing nature of cancer poses the most difficult challenge oncologists face today. Cancer's remarkable adaptability has inspired many to work toward understanding the evolutionary dynamics that underlie this disease in hopes of learning new ways to fight it. Eco-evolutionary dynamics of a tumor are not accounted for in most standard treatment regimens, but exploiting them would help us combat treatment-resistant effectively. Here, we outline several notable efforts to exploit these dynamics and circumvent drug resistance in cancer.
MeSH term(s)	Humans ; Neoplasms/drug therapy ; Neoplasms/genetics ; Neoplasms/pathology ; Drug Resistance ; Biological Evolution
Language	English
Publishing date	2023-04-04
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms24076738
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Article: Exploiting convergent phenotypes to derive a pan-cancer cisplatin response gene expression signature.

Scarborough, Jessica A / Eschrich, Steven A / Torres-Roca, Javier / Dhawan, Andrew / Scott, Jacob G

NPJ precision oncology

2023 Volume 7, Issue 1, Page(s) 38

Abstract: Precision medicine offers remarkable potential for the treatment of cancer, but is largely focused on tumors that harbor actionable mutations. Gene expression signatures can expand the scope of precision medicine by predicting response to traditional ( ... ...

Abstract	Precision medicine offers remarkable potential for the treatment of cancer, but is largely focused on tumors that harbor actionable mutations. Gene expression signatures can expand the scope of precision medicine by predicting response to traditional (cytotoxic) chemotherapy agents without relying on changes in mutational status. We present a new signature extraction method, inspired by the principle of convergent phenotypes, which states that tumors with disparate genetic backgrounds may evolve similar phenotypes independently. This evolutionary-informed method can be utilized to produce consensus signatures predictive of response to over 200 chemotherapeutic drugs found in the Genomics of Drug Sensitivity in Cancer (GDSC) Database. Here, we demonstrate its use by extracting the Cisplatin Response Signature (CisSig). We show that this signature can predict cisplatin response within carcinoma-based cell lines from the GDSC database, and expression of the signatures aligns with clinical trends seen in independent datasets of tumor samples from The Cancer Genome Atlas (TCGA) and Total Cancer Care (TCC) database. Finally, we demonstrate preliminary validation of CisSig for use in muscle-invasive bladder cancer, predicting overall survival in a small cohort of patients who undergo cisplatin-containing chemotherapy. This methodology can be used to produce robust signatures that, with further clinical validation, may be used for the prediction of traditional chemotherapeutic response, dramatically increasing the reach of personalized medicine in cancer.
Language	English
Publishing date	2023-04-19
Publishing country	England
Document type	Journal Article
ISSN	2397-768X
ISSN	2397-768X
DOI	10.1038/s41698-023-00375-y
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Article ; Online: Revisiting a Null Hypothesis: Exploring the Parameters of Oligometastasis Treatment.

Scarborough, Jessica A / Tom, Martin C / Kattan, Michael W / Scott, Jacob G

International journal of radiation oncology, biology, physics

2021 Volume 110, Issue 2, Page(s) 371–381

Abstract: Purpose: In the treatment of patients with metastatic cancer, the current paradigm states that metastasis-directed therapy does not prolong life. This paradigm forms the basis of clinical trial null hypotheses, where trials are built to test the null ... ...

Abstract	Purpose: In the treatment of patients with metastatic cancer, the current paradigm states that metastasis-directed therapy does not prolong life. This paradigm forms the basis of clinical trial null hypotheses, where trials are built to test the null hypothesis that patients garner no overall survival benefit from targeting metastatic lesions. However, with advancing imaging technology and increasingly precise techniques for targeting lesions, a much larger proportion of metastatic disease can be treated. As a result, the life-extending benefit of targeting metastatic disease is becoming increasingly clear. Methods and materials: In this work, we suggest shifting this qualitative null hypothesis and describe a mathematical model that can be used to frame a new, quantitative null. We begin with a very simple formulation of tumor growth, an exponential function, and illustrate how the same intervention (removing a given number of cells from the tumor) at different times affects survival. Additionally, we postulate where recent clinical trials fit into this parameter space and discuss the implications of clinical trial design in changing these quantitative parameters. Results: Our model shows that although any amount of cell kill will extend survival, in many cases the extent is so small as to be unnoticeable in a clinical context or is outweighed by factors related to toxicity and treatment time. Conclusions: Recasting the null in these quantitative terms will allow trialists to design trials specifically to increase understanding of the circumstances (patient selection, disease burden, tumor growth kinetics) that can lead to improved overall survival when targeting metastatic lesions, rather than whether targeting metastases extends survival for patients with (oligo-) metastatic disease.
MeSH term(s)	Clinical Trials as Topic ; Growth ; Humans ; Models, Theoretical ; Neoplasm Metastasis/diagnostic imaging ; Neoplasm Metastasis/pathology ; Neoplasm Metastasis/radiotherapy ; Neoplasms/mortality ; Neoplasms/pathology ; Research Design ; Statistics as Topic ; Time Factors
Language	English
Publishing date	2021-01-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	197614-x
ISSN	1879-355X ; 0360-3016
ISSN (online)	1879-355X
ISSN	0360-3016
DOI	10.1016/j.ijrobp.2020.12.044
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Article ; Online: Radiotherapy with genomic-adjusted radiation dose - Authors' reply.

Scott, Jacob G / Sedor, Geoffrey / Scarborough, Jessica A / Kattan, Michael W / Torres-Roca, Javier F

The Lancet. Oncology

2021 Volume 22, Issue 11, Page(s) e470–e471

MeSH term(s)	Dose Fractionation, Radiation ; Genomics ; Humans ; Radiation Dosage ; Radiation Oncology
Language	English
Publishing date	2021-10-08
Publishing country	England
Document type	Letter ; Comment
ZDB-ID	2049730-1
ISSN	1474-5488 ; 1470-2045
ISSN (online)	1474-5488
ISSN	1470-2045
DOI	10.1016/S1470-2045(21)00601-X
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Article ; Online: Evolution of the ability to modulate host chemokine networks via gene duplication in human cytomegalovirus (HCMV).

Scarborough, Jessica A / Paul, John R / Spencer, Juliet V

Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases

2017 Volume 51, Page(s) 46–53

Abstract: Human cytomegalovirus (HCMV) is a widespread pathogen that is particularly skillful at evading immune detection and defense mechanisms, largely due to extensive co-evolution with its host. One aspect of this co-evolution involves the acquisition of ... ...

Abstract	Human cytomegalovirus (HCMV) is a widespread pathogen that is particularly skillful at evading immune detection and defense mechanisms, largely due to extensive co-evolution with its host. One aspect of this co-evolution involves the acquisition of virally encoded G protein-coupled receptors (GPCRs) with homology to the chemokine receptor family. GPCRs are the largest family of cell surface proteins, found in organisms from yeast to humans, and they regulate a variety of cellular processes including development, sensory perception, and immune cell trafficking. The US27 and US28 genes are encoded by human and primate CMVs, but homologs are not found in the genomes of viruses infecting rodents or other species. Phylogenetic analysis was used to investigate the US27 and US28 genes, which are adjacent in the unique short (US) region of the HCMV genome, and their relationship to one another and to human chemokine receptor genes. The results indicate that both US27 and US28 share the same common ancestor with human chemokine receptor CX3CR1, suggesting that a single host gene was captured and a subsequent viral gene duplication event occurred. The US28 gene product (pUS28) has maintained the function of the ancestral gene and has the ability to bind and signal in response to CX3CL1/fractalkine, the natural ligand for CX3CR1. In contrast, pUS27 does not bind to any known chemokine ligand, and the sequence has diverged significantly, highlighted by the fact that pUS27 currently exhibits greater sequence similarity to human CCR1. While the evolutionary advantage of the gene duplication and neofunctionalization event remains unclear, the US27 and US28 genes are highly conserved among different HCMV strains and retained even in laboratory strains that have lost many virulence genes, suggesting that US27 and US28 have each evolved distinct, important functions during virus infection.
MeSH term(s)	Biological Coevolution ; CX3C Chemokine Receptor 1/genetics ; CX3C Chemokine Receptor 1/metabolism ; Chemokine CX3CL1/genetics ; Chemokine CX3CL1/metabolism ; Cytomegalovirus/classification ; Cytomegalovirus/genetics ; Cytomegalovirus/metabolism ; Cytomegalovirus Infections/virology ; Gene Duplication ; Gene Expression Regulation ; Genome, Viral ; Host-Pathogen Interactions/genetics ; Humans ; Molecular Mimicry ; Phylogeny ; Receptors, CCR1/genetics ; Receptors, CCR1/metabolism ; Receptors, Chemokine/genetics ; Receptors, Chemokine/metabolism ; Signal Transduction ; Viral Proteins/genetics ; Viral Proteins/metabolism
Chemical Substances	CCR1 protein, human ; CX3C Chemokine Receptor 1 ; CX3CL1 protein, human ; CX3CR1 protein, human ; Chemokine CX3CL1 ; Receptors, CCR1 ; Receptors, Chemokine ; US27 protein, human cytomegalovirus ; US28 receptor, Cytomegalovirus ; Viral Proteins
Language	English
Publishing date	2017-03-14
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2037068-4
ISSN	1567-7257 ; 1567-1348
ISSN (online)	1567-7257
ISSN	1567-1348
DOI	10.1016/j.meegid.2017.03.013
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Article ; Online: SLX4IP promotes RAP1 SUMOylation by PIAS1 to coordinate telomere maintenance through NF-κB and Notch signaling.

Robinson, Nathaniel J / Miyagi, Masaru / Scarborough, Jessica A / Scott, Jacob G / Taylor, Derek J / Schiemann, William P

Science signaling

2021 Volume 14, Issue 689

Abstract: The maintenance of telomere length supports repetitive cell division and therefore plays a central role in cancer development and progression. Telomeres are extended by either the enzyme telomerase or the alternative lengthening of telomeres (ALT) ... ...

Abstract	The maintenance of telomere length supports repetitive cell division and therefore plays a central role in cancer development and progression. Telomeres are extended by either the enzyme telomerase or the alternative lengthening of telomeres (ALT) pathway. Here, we found that the telomere-associated protein SLX4IP dictates telomere proteome composition by recruiting and activating the E3 SUMO ligase PIAS1 to the SLX4 complex. PIAS1 SUMOylated the telomere-binding protein RAP1, which disrupted its interaction with the telomere-binding protein TRF2 and facilitated its nucleocytoplasmic shuttling. In the cytosol, RAP1 bound to IκB kinase (IKK), resulting in activation of the transcription factor NF-κB and its induction of
MeSH term(s)	Animals ; Carrier Proteins/genetics ; Cell Line, Tumor ; Mice ; NF-kappa B/genetics ; Protein Inhibitors of Activated STAT/metabolism ; Receptors, Notch ; Signal Transduction ; Sumoylation ; Telomerase/genetics ; Telomerase/metabolism ; Telomere/genetics ; Telomere/metabolism ; Ubiquitin-Protein Ligases/metabolism ; rap1 GTP-Binding Proteins/metabolism
Chemical Substances	Carrier Proteins ; NF-kappa B ; Pias1 protein, mouse ; Protein Inhibitors of Activated STAT ; Receptors, Notch ; Ubiquitin-Protein Ligases (EC 2.3.2.27) ; Telomerase (EC 2.7.7.49) ; Rap1 protein, mouse (EC 3.6.5.2) ; rap1 GTP-Binding Proteins (EC 3.6.5.2)
Language	English
Publishing date	2021-06-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2417226-1
ISSN	1937-9145 ; 1945-0877
ISSN (online)	1937-9145
ISSN	1945-0877
DOI	10.1126/scisignal.abe9613
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Article: A clinicogenomic model including GARD predicts outcome for radiation treated patients with HPV+ oropharyngeal squamous cell carcinoma.

Ho, Emily / De Cecco, Loris / Cavalieri, Stefano / Sedor, Geoffrey / Hoebers, Frank / Brakenhoff, Ruud H / Scheckenbach, Kathrin / Poli, Tito / Yang, Kailin / Scarborough, Jessica A / Campbell, Shauna / Koyfman, Shlomo / Eschrich, Steven A / Caudell, Jimmy J / Kattan, Michael W / Licitra, Lisa / Torres-Roca, Javier F / Scott, Jacob G

medRxiv : the preprint server for health sciences

2023

Abstract: Background: Treatment decision-making in oropharyngeal squamous cell carcinoma (OPSCC) includes clinical stage, HPV status, and smoking history. Despite improvements in staging with separation of HPV-positive and -negative OPSCC in AJCC 8th edition ( ... ...

Abstract	Background: Treatment decision-making in oropharyngeal squamous cell carcinoma (OPSCC) includes clinical stage, HPV status, and smoking history. Despite improvements in staging with separation of HPV-positive and -negative OPSCC in AJCC 8th edition (AJCC8), patients are largely treated with a uniform approach, with recent efforts focused on de-intensification in low-risk patients. We have previously shown, in a pooled analysis, that the genomic adjusted radiation dose (GARD) is predictive of radiation treatment benefit and can be used to guide RT dose selection. We hypothesize that GARD can be used to predict overall survival (OS) in HPV-positive OPSCC patients treated with radiotherapy (RT). Methods: Gene expression profiles (Affymetrix Clariom D) were analyzed for 234 formalin-fixed paraffin-embedded samples from HPV-positive OPSCC patients within an international, multi-institutional, prospective/retrospective observational study including patients with AJCC 7th edition stage III-IVb. GARD, a measure of the treatment effect of RT, was calculated for each patient as previously described. In total, 191 patients received primary RT definitive treatment (chemoradiation or RT alone, and 43 patients received post-operative RT. Two RT dose fractionations were utilized for primary RT cases (70 Gy in 35 fractions or 69.96 Gy in 33 fractions). Median RT dose was 70 Gy (range 50.88-74) for primary RT definitive cases and 66 Gy (range 44-70) for post-operative RT cases. The median follow up was 46.2 months (95% CI, 33.5-63.1). Cox proportional hazards analyses were performed with GARD as both a continuous and dichotomous variable and time-dependent ROC analyses compared the performance of GARD with the NRG clinical nomogram for overall survival. Results: Despite uniform radiation dose utilization, GARD showed significant heterogeneity (range 30-110), reflecting the underlying genomic differences in the cohort. On multivariable analysis, each unit increase in GARD was associated with an improvement in OS (HR = 0.951 (0.911, 0.993), p = 0.023) compared to AJCC8 (HR = 1.999 (0.791, 5.047)), p = 0.143). ROC analysis for GARD at 36 months yielded an AUC of 80.6 (69.4, 91.9) compared with an AUC of 73.6 (55.4, 91.7) for the NRG clinical nomogram. GARD≥64.2 was associated with improved OS (HR = 0.280 (0.100, 0.781), p = 0.015). In a virtual trial, GARD predicts that uniform RT dose de-escalation results in overall inferior OS but proposes two separate genomic strategies where selective RT dose de-escalation in GARD-selected populations results in clinical equipoise. Conclusions: In this multi-institutional cohort of patients with HPV-positive OPSCC, GARD predicts OS as a continuous variable, outperforms the NRG nomogram and provides a novel genomic strategy to modern clinical trial design. We propose that GARD, which provides the first opportunity for genomic guided personalization of radiation dose, should be incorporated in the diagnostic workup of HPV-positive OPSCC patients.
Language	English
Publishing date	2023-09-14
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.09.14.23295538
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Article ; Online: Identifying States of Collateral Sensitivity during the Evolution of Therapeutic Resistance in Ewing's Sarcoma.

Scarborough, Jessica A / McClure, Erin / Anderson, Peter / Dhawan, Andrew / Durmaz, Arda / Lessnick, Stephen L / Hitomi, Masahiro / Scott, Jacob G

iScience

2020 Volume 23, Issue 7, Page(s) 101293

Abstract: Advances in the treatment of Ewing's sarcoma (EWS) are desperately needed, particularly in the case of metastatic disease. A deeper understanding of collateral sensitivity, where the evolution of therapeutic resistance to one drug aligns with sensitivity ...

Abstract	Advances in the treatment of Ewing's sarcoma (EWS) are desperately needed, particularly in the case of metastatic disease. A deeper understanding of collateral sensitivity, where the evolution of therapeutic resistance to one drug aligns with sensitivity to another drug, may improve our ability to effectively target this disease. For the first time in a solid tumor, we produced a temporal collateral sensitivity map that demonstrates the evolution of collateral sensitivity and resistance in EWS. We found that the evolution of collateral resistance was predictable with some drugs but had significant variation in response to other drugs. Using this map of temporal collateral sensitivity in EWS, we can see that the path toward collateral sensitivity is not always repeatable, nor is there always a clear trajectory toward resistance or sensitivity. Identifying transcriptomic changes that accompany these states of transient collateral sensitivity could improve treatment planning for patients with EWS.
Language	English
Publishing date	2020-06-20
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2020.101293
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Article: Evolution of the ability to modulate host chemokine networks via gene duplication in human cytomegalovirus (HCMV)

Scarborough, Jessica A / John R. Paul / Juliet V. Spencer

Infection, genetics, and evolution. 2017 July, v. 51

2017

Abstract	Human cytomegalovirus (HCMV) is a widespread pathogen that is particularly skillful at evading immune detection and defense mechanisms, largely due to extensive co-evolution with its host. One aspect of this co-evolution involves the acquisition of virally encoded G protein-coupled receptors (GPCRs) with homology to the chemokine receptor family. GPCRs are the largest family of cell surface proteins, found in organisms from yeast to humans, and they regulate a variety of cellular processes including development, sensory perception, and immune cell trafficking. The US27 and US28 genes are encoded by human and primate CMVs, but homologs are not found in the genomes of viruses infecting rodents or other species. Phylogenetic analysis was used to investigate the US27 and US28 genes, which are adjacent in the unique short (US) region of the HCMV genome, and their relationship to one another and to human chemokine receptor genes. The results indicate that both US27 and US28 share the same common ancestor with human chemokine receptor CX3CR1, suggesting that a single host gene was captured and a subsequent viral gene duplication event occurred. The US28 gene product (pUS28) has maintained the function of the ancestral gene and has the ability to bind and signal in response to CX3CL1/fractalkine, the natural ligand for CX3CR1. In contrast, pUS27 does not bind to any known chemokine ligand, and the sequence has diverged significantly, highlighted by the fact that pUS27 currently exhibits greater sequence similarity to human CCR1. While the evolutionary advantage of the gene duplication and neofunctionalization event remains unclear, the US27 and US28 genes are highly conserved among different HCMV strains and retained even in laboratory strains that have lost many virulence genes, suggesting that US27 and US28 have each evolved distinct, important functions during virus infection.
Keywords	CCR1 receptor ; chemokines ; coevolution ; defense mechanisms ; gene duplication ; genes ; Human herpesvirus 5 ; humans ; ligands ; pathogens ; phylogeny ; rodents ; sensation ; sequence homology ; surface proteins ; virulence ; viruses ; yeasts
Language	English
Dates of publication	2017-07
Size	p. 46-53.
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	2037068-4
ISSN	1567-1348
ISSN	1567-1348
DOI	10.1016/j.meegid.2017.03.013
Database	NAL-Catalogue (AGRICOLA)

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