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Article: Dynamic Monitoring of EMT in CTCs as an Indicator of Cancer Metastasis

Zhang, Zhen / Wuethrich, Alain / Wang, Jing / Korbie, Darren / Lin, Lynlee L. / Trau, Matt

Analytical chemistry. 2021 Dec. 10, v. 93, no. 50

2021

Abstract: Epithelial to mesenchymal transition (EMT) results in the genesis of circulating tumor cells (CTCs) from tumor sites and promotes the metastatic capability of CTCs in circulation. In this study, we develop a multiplex surface-enhanced Raman scattering ... ...

Abstract	Epithelial to mesenchymal transition (EMT) results in the genesis of circulating tumor cells (CTCs) from tumor sites and promotes the metastatic capability of CTCs in circulation. In this study, we develop a multiplex surface-enhanced Raman scattering nanotechnology for comprehensive characterization of EMT-associated phenotypes in CTCs, to monitor cancer metastasis. We observe the downregulation of the CTC marker (EpCAM) and the epithelial marker (E-cadherin), as well as the upregulation of a mesenchymal marker (N-cadherin) and a stem cell marker (ABCB5) during the transforming growth factor-β-induced EMT process in breast cancer cell line models. Additionally, we also find changes in the heterogeneity levels of these selected markers in cells. With this method, we successfully detect the presence of disease in samples from breast cancer patients and characterize EMT-associated phenotypes in their CTCs. Overall, this approach and findings provide a new means for monitoring the EMT process in cancer, insights into the detailed mechanistic progress of the diseases, and have potential for detecting the early occurrence of cancer metastasis.
Keywords	analytical chemistry ; breast neoplasms ; cadherins ; cell lines ; epithelium ; metastasis ; neoplasm cells ; stem cells
Language	English
Dates of publication	2021-1210
Size	p. 16787-16795.
Publishing place	American Chemical Society
Document type	Article
ZDB-ID	1508-8
ISSN	1520-6882 ; 0003-2700
ISSN (online)	1520-6882
ISSN	0003-2700
DOI	10.1021/acs.analchem.1c03167
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Dynamic Monitoring of EMT in CTCs as an Indicator of Cancer Metastasis.

Zhang, Zhen / Wuethrich, Alain / Wang, Jing / Korbie, Darren / Lin, Lynlee L / Trau, Matt

Analytical chemistry

2021 Volume 93, Issue 50, Page(s) 16787–16795

Abstract	Epithelial to mesenchymal transition (EMT) results in the genesis of circulating tumor cells (CTCs) from tumor sites and promotes the metastatic capability of CTCs in circulation. In this study, we develop a multiplex surface-enhanced Raman scattering nanotechnology for comprehensive characterization of EMT-associated phenotypes in CTCs, to monitor cancer metastasis. We observe the downregulation of the CTC marker (EpCAM) and the epithelial marker (E-cadherin), as well as the upregulation of a mesenchymal marker (N-cadherin) and a stem cell marker (ABCB5) during the transforming growth factor-β-induced EMT process in breast cancer cell line models. Additionally, we also find changes in the heterogeneity levels of these selected markers in cells. With this method, we successfully detect the presence of disease in samples from breast cancer patients and characterize EMT-associated phenotypes in their CTCs. Overall, this approach and findings provide a new means for monitoring the EMT process in cancer, insights into the detailed mechanistic progress of the diseases, and have potential for detecting the early occurrence of cancer metastasis.
MeSH term(s)	Epithelial-Mesenchymal Transition ; Humans ; Neoplasms
Language	English
Publishing date	2021-12-10
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1508-8
ISSN	1520-6882 ; 0003-2700
ISSN (online)	1520-6882
ISSN	0003-2700
DOI	10.1021/acs.analchem.1c03167
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Article ; Online: SERS Multiplex Profiling of Melanoma Circulating Tumor Cells for Predicting the Response to Immune Checkpoint Blockade Therapy.

Li, Junrong / Wuethrich, Alain / Zhang, Zhen / Wang, Jing / Lin, Lynlee L / Behren, Andreas / Wang, Yuling / Trau, Matt

Analytical chemistry

2022 Volume 94, Issue 42, Page(s) 14573–14582

Abstract: Immune checkpoint blockade (ICB) therapy has achieved remarkable success in many cancers including melanoma. However, ICB therapy benefits only a small proportion of patients and produces severe side effects for some patients. Thus, there is an urgent ... ...

Abstract	Immune checkpoint blockade (ICB) therapy has achieved remarkable success in many cancers including melanoma. However, ICB therapy benefits only a small proportion of patients and produces severe side effects for some patients. Thus, there is an urgent need to identify patients who are more likely to respond to ICB therapy to improve outcomes and minimize side effects. To predict ICB therapy responses, we design a surface-enhanced Raman scattering (SERS) assay for multiplex profiling of circulating tumor cells (CTCs) under basal and interferon-γ (IFN-γ) stimulation. Through simultaneous ensemble and single-cell measurements of CTCs, the SERS assay can reveal tumor heterogeneity and offer a comprehensive CTC phenotype for decision-making. Anisotropic gold-silver alloy nanoboxes are utilized as SERS plasmonic substrates for improved signal readouts of CTC surface biomarkers. By generating a unique CTC signature with four surface biomarkers, the developed assay enables the differentiation of CTCs from three different patient-derived melanoma cell lines. Significantly, in a cohort of 14 melanoma patients who received programmed cell death-1 blockade therapy, the changes of CTC signature induced by IFN-γ stimulation to CTCs show the potential to predict responders. We expect that the SERS assay can help select patients for receiving ICB therapy in other cancers.
MeSH term(s)	Humans ; Neoplastic Cells, Circulating ; Immune Checkpoint Inhibitors ; Silver ; Interferon-gamma ; Melanoma/drug therapy ; Melanoma/pathology ; Gold ; Biomarkers ; Alloys
Chemical Substances	Immune Checkpoint Inhibitors ; Silver (3M4G523W1G) ; Interferon-gamma (82115-62-6) ; Gold (7440-57-5) ; Biomarkers ; Alloys
Language	English
Publishing date	2022-10-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1508-8
ISSN	1520-6882 ; 0003-2700
ISSN (online)	1520-6882
ISSN	0003-2700
DOI	10.1021/acs.analchem.2c02398
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Article ; Online: Cytokine/Chemokine assessment as a complementary diagnostic tool for inflammatory skin diseases.

Liu, Timothy J / Lin, Lynlee L / McMeniman, Erin / Wu, Jason / Kao, Yung-Ching / Kumari, Snehlata / Boyle, Glen M / Wells, James W / Soyer, H Peter / Gonzalez-Cruz, Jazmina L

Frontiers in immunology

2022 Volume 13, Page(s) 1028435

Abstract: Inflammatory skin conditions are the ... ...

Abstract	Inflammatory skin conditions are the 4
MeSH term(s)	Humans ; Cytokines ; Dermatitis, Atopic/diagnosis ; Pilot Projects ; Chemokines ; Psoriasis/diagnosis
Chemical Substances	Cytokines ; Chemokines
Language	English
Publishing date	2022-11-16
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.1028435
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Article ; Online: Changes in the skin microbiome associated with squamous cell carcinoma in transplant recipients.

Krueger, Annika / Zaugg, Julian / Lachner, Nancy / Bialasiewicz, Seweryn / Lin, Lynlee L / Gabizon, Sharon / Sobarun, Priyamvada / Morrison, Mark / Soyer, H Peter / Hugenholtz, Philip / Frazer, Ian H

ISME communications

2022 Volume 2, Issue 1, Page(s) 13

Abstract: Actinic keratoses (AK) arise in severely photo-damaged skin and can progress to squamous cell carcinomas (SCC). AK and SCC are common in Caucasian populations, and immunosuppressed individuals have a markedly higher risk of developing SCC. An ... ...

Abstract	Actinic keratoses (AK) arise in severely photo-damaged skin and can progress to squamous cell carcinomas (SCC). AK and SCC are common in Caucasian populations, and immunosuppressed individuals have a markedly higher risk of developing SCC. An overabundance of Staphylococcus aureus has been reported in AK and SCC lesions of immunocompetent individuals, however, the AK/SCC microbiome in immunosuppressed cohorts has not been investigated. Here, the microbial profile and bacterial load of AK, SCC and control skin swabs from 32 immunosuppressed organ transplant recipients were characterised via SSU rRNA gene sequencing and qPCR, and compared to a previously described immunocompetent cohort. Although the taxonomic composition of skin swab samples was mostly subject-specific, significant differences were observed between control skin, AK, and SCC in both cohorts. Surface bacterial load was increased and alpha diversity decreased in AK and SCC compared to control skin due to an increased abundance of Staphylococcus species and relative decrease of skin commensals. Staphylococcus epidermidis predominated on SCC from transplant recipients in contrast to SCC of immunocompetent subjects dominated by S. aureus. In conclusion, AK and SCC of immunosuppressed and immunocompetent subjects present with distinctive microbial dysbioses, which may be relevant to SCC pathogenesis and progression.
Language	English
Publishing date	2022-02-01
Publishing country	England
Document type	Journal Article
ISSN	2730-6151
ISSN (online)	2730-6151
DOI	10.1038/s43705-022-00095-7
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Article ; Online: Tracking Drug-Induced Epithelial-Mesenchymal Transition in Breast Cancer by a Microfluidic Surface-Enhanced Raman Spectroscopy Immunoassay.

Zhang, Zhen / Wang, Jing / Shanmugasundaram, Karthik Balaji / Yeo, Belinda / Möller, Andreas / Wuethrich, Alain / Lin, Lynlee L / Trau, Matt

Small (Weinheim an der Bergstrasse, Germany)

2020 Volume 16, Issue 13, Page(s) e1905614

Abstract: Epithelial-mesenchymal transition (EMT) is a primary mechanism for cancer metastasis. Detecting the activation of EMT can potentially convey signs of metastasis to guide treatment management and improve patient survival. One of the classic signatures of ... ...

Abstract	Epithelial-mesenchymal transition (EMT) is a primary mechanism for cancer metastasis. Detecting the activation of EMT can potentially convey signs of metastasis to guide treatment management and improve patient survival. One of the classic signatures of EMT is characterized by dynamic changes in cellular expression levels of E-cadherin and N-cadherin, whose soluble active fragments have recently been reported to be biomarkers for cancer diagnosis and prognosis. Herein, a microfluidic immunoassay (termed "SERS immunoassay") based on sensitive and simultaneous detection of soluble E-cadherin (sE-cadherin) and soluble N-cadherin (sN-cadherin) for EMT monitoring in patients' plasma is presented. The SERS immunoassay integrates in situ nanomixing and surface-enhanced Raman scattering readout to enable accurate detection of sE-cadherin and sN-cadherin from as low as 10 cells mL
MeSH term(s)	Breast Neoplasms/physiopathology ; Cadherins/metabolism ; Cell Line, Tumor ; Epithelial-Mesenchymal Transition/drug effects ; Humans ; Immunoassay ; Microfluidics ; Pharmaceutical Preparations ; Spectrum Analysis, Raman
Chemical Substances	Cadherins ; Pharmaceutical Preparations
Language	English
Publishing date	2020-03-05
Publishing country	Germany
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2168935-0
ISSN	1613-6829 ; 1613-6810
ISSN (online)	1613-6829
ISSN	1613-6810
DOI	10.1002/smll.201905614
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Tracking extracellular vesicle phenotypic changes enables treatment monitoring in melanoma.

Wang, Jing / Wuethrich, Alain / Sina, Abu Ali Ibn / Lane, Rebecca E / Lin, Lynlee L / Wang, Yuling / Cebon, Jonathan / Behren, Andreas / Trau, Matt

Science advances

2020 Volume 6, Issue 9, Page(s) eaax3223

Abstract: Monitoring targeted therapy in real time for cancer patients could provide vital information about the development of drug resistance and improve therapeutic outcomes. Extracellular vesicles (EVs) have recently emerged as a promising cancer biomarker, ... ...

Abstract	Monitoring targeted therapy in real time for cancer patients could provide vital information about the development of drug resistance and improve therapeutic outcomes. Extracellular vesicles (EVs) have recently emerged as a promising cancer biomarker, and EV phenotyping shows high potential for monitoring treatment responses. Here, we demonstrate the feasibility of monitoring patient treatment responses based on the plasma EV phenotypic evolution using a multiplex EV phenotype analyzer chip (EPAC). EPAC incorporates the nanomixing-enhanced microchip and the multiplex surface-enhanced Raman scattering (SERS) nanotag system for direct EV phenotyping without EV enrichment. In a preclinical model, we observe the EV phenotypic heterogeneity and different phenotypic responses to the treatment. Furthermore, we successfully detect cancer-specific EV phenotypes from melanoma patient plasma. We longitudinally monitor the EV phenotypic evolution of eight melanoma patients receiving targeted therapy and find specific EV profiles involved in the development of drug resistance, reflecting the potential of EV phenotyping for monitoring treatment responses.
MeSH term(s)	Cell Line, Tumor ; Extracellular Vesicles/metabolism ; Extracellular Vesicles/pathology ; Female ; Humans ; Male ; Melanoma/blood ; Melanoma/pathology ; Melanoma/therapy ; Microarray Analysis ; Spectrum Analysis, Raman
Language	English
Publishing date	2020-02-26
Publishing country	United States
Document type	Clinical Trial ; Journal Article ; Multicenter Study ; Research Support, Non-U.S. Gov't
ZDB-ID	2810933-8
ISSN	2375-2548 ; 2375-2548
ISSN (online)	2375-2548
ISSN	2375-2548
DOI	10.1126/sciadv.aax3223
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Article ; Online: A minimally invasive clinical model to test sunscreen toxicity based on oxidative stress levels using microbiopsy and confocal microscopy - a proof of concept study.

Yamada, Miko / Lin, Lynlee L / Hang, Lydia Y T / Belt, Paul J / Peter Soyer, H / Raphael, Anthony P / Prow, Tarl W

International journal of cosmetic science

2020 Volume 42, Issue 5, Page(s) 462–470

Abstract: Objective: This proof-of-concept study demonstrated that using minimally invasive skin microsampling could enable significantly higher throughput of cosmetic testing in volunteers than conventional biopsy. Nanoparticle sunscreen was used as a model to ... ...

Abstract	Objective: This proof-of-concept study demonstrated that using minimally invasive skin microsampling could enable significantly higher throughput of cosmetic testing in volunteers than conventional biopsy. Nanoparticle sunscreen was used as a model to test toxicity based on oxidative stress using microbiopsy and confocal imaging. Methods: Six volunteers were recruited for this study (3 males and 3 females). Zinc oxide nanoparticle containing topical formulation was prepared at 10% w/v. Each volunteer had 3 areas of 4 cm Results: Skin exposed to zinc oxide nanoparticles did not show any significant increases in oxidative stress. Zinc oxide nanoparticle tape-stripped skin resulted in signal significantly lower (P < 0.001) oxidative stress levels than t-butylated hydroxytoluene treated tape-stripped skin for oxidative stress markers. Topically applied zinc oxide nanoparticles had no detectable effect on the oxidative status in volunteer skin. No adverse reactions or effects were observed after all treatments including microbiopsy. Conclusion: The data support the hypothesis that microbiopsy is a viable approach to study cosmeceutical- skin interactions in volunteers with capacity for molecular assays and high throughput with very low risk to the volunteer.
MeSH term(s)	Biopsy/methods ; Humans ; Metal Nanoparticles/chemistry ; Microscopy, Confocal/methods ; Oxidative Stress ; Proof of Concept Study ; Sunscreening Agents/toxicity ; Zinc Oxide/administration & dosage
Chemical Substances	Sunscreening Agents ; Zinc Oxide (SOI2LOH54Z)
Language	English
Publishing date	2020-08-30
Publishing country	England
Document type	Journal Article
ZDB-ID	198917-0
ISSN	1468-2494 ; 0142-5463
ISSN (online)	1468-2494
ISSN	0142-5463
DOI	10.1111/ics.12646
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: A high-resolution study of in situ surface-enhanced Raman scattering nanotag behavior in biological systems.

Wang, Jing / Anderson, Will / Li, Junrong / Lin, Lynlee L / Wang, Yuling / Trau, Matt

Journal of colloid and interface science

2018 Volume 537, Page(s) 536–546

Abstract: The colloidal stability of surface-enhanced Raman scattering (SERS) nanotags (Raman reporter-conjugated plasmonic nanoparticles) significantly affects the accuracy and reproducibility of SERS measurements, particularly in biological systems. Limited ... ...

Abstract	The colloidal stability of surface-enhanced Raman scattering (SERS) nanotags (Raman reporter-conjugated plasmonic nanoparticles) significantly affects the accuracy and reproducibility of SERS measurements, particularly in biological systems. Limited understanding of SERS nanotag stability may partly hamper the translation of SERS nanotags from the laboratory to their use in the clinic. In this contribution, we utilized differential centrifugal sedimentation (DCS), a reliable and straightforward technique to comprehensively analyze the colloidal stability of SERS nanotags in biological systems. Compared with other particle characterization techniques, DCS has been shown to have a unique advantage for high-resolution and high-throughput polydisperse particle characterization. DCS data revealed that the universal aggregation prevention practice of coating SERS nanotags with silica or bovine serum albumin layers did not sufficiently stabilize them in common measurement environments (e.g., 1 × PBS). Combined DCS and SERS measurements established a strong correlation between the degrees of nanotag aggregation and signal intensities, further reinforcing the necessity of characterizing SERS nanotag stability for every condition in which they are used. We also found that increasing the protein thickness by the inclusion of extra protein components in the detection environments and antibody functionalization can improve the stability of SERS nanotags. We believe that this study can provide guidelines on appropriate measurement techniques and particle design considerations to assess and improve SERS nanotag stability in complex biological systems.
MeSH term(s)	Animals ; Benzoates/chemistry ; Cattle ; Gold/chemistry ; Humans ; Nanoparticles/chemistry ; Particle Size ; Serum Albumin, Bovine/chemistry ; Silicon Dioxide/chemistry ; Spectrum Analysis, Raman ; Sulfhydryl Compounds/chemistry ; Surface Properties
Chemical Substances	Benzoates ; Sulfhydryl Compounds ; 4-mercaptobenzoate (1074-36-8) ; Serum Albumin, Bovine (27432CM55Q) ; Gold (7440-57-5) ; Silicon Dioxide (7631-86-9)
Language	English
Publishing date	2018-11-12
Publishing country	United States
Document type	Journal Article
ZDB-ID	241597-5
ISSN	1095-7103 ; 0021-9797
ISSN (online)	1095-7103
ISSN	0021-9797
DOI	10.1016/j.jcis.2018.11.035
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Article ; Online: The opportunity for microbiopsies for skin cancer.

Prow, Tarl W / Lin, Lynlee L / Soyer, H Peter

Future oncology (London, England)

2013 Volume 9, Issue 9, Page(s) 1241–1243

MeSH term(s)	Biopsy, Needle ; Humans ; Skin Neoplasms/pathology
Language	English
Publishing date	2013-09
Publishing country	England
Document type	Editorial
ZDB-ID	2184533-5
ISSN	1744-8301 ; 1479-6694
ISSN (online)	1744-8301
ISSN	1479-6694
DOI	10.2217/fon.13.88
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