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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Oncology".

Deadline for manuscript submissions: closed (31 May 2021) | Viewed by 28521

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Dr. Stefano Indraccolo

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Immunology and Molecular Oncology Unit, Veneto Institute of Oncology IOV—IRCCS, 35128 Padova, Italy
Interests: translational research; lung cancer and ovarian cancer; notch signaling in cancer; tumor angiogenesis and metabolism; mechanisms of resistance to antiangiogenic therapy; prognostic/predictive biomarker identification
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Dr. Paola Ulivi

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Biosciences Laboratory, IRCCS Istituto Romagnolo per lo Studio dei Tumori “Dino Amadori” (IRST), via P. Maroncelli 40, 47014 Meldola, Italy
Interests: translational research; biomarkers; liquid biopsy; oncology
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Liquid biopsy has emerged as new tool for detecting clinically relevant genetic alterations in cancer patients. The term liquid biopsy is commonly used not only to refer to molecular assays performed on cell-free DNA purified from plasma but can also include testing on other body fluids, such as urine and cerebrospinal fluid and measurements of circulating tumor cells, exosomes and circulating tumor RNA.

Here, we would like to focus on liquid biopsy approaches to track response to therapy in solid tumors. This special issue will cover studies investigating the significance of liquid biopsy for diagnostic/prognostic purposes as well as to predict patient outcome, compared with patient management guided via canonical molecular data and imaging modalities.

In this Special Issue, we welcome Original Research and Review articles focused on, but not limited to, dynamic measurements of mutations and other genetic alterations in plasma or other fluids. Studies on other liquid biopsy biomarkers such as microRNA and proteins are also considered.

You may choose our Joint Special Issue in Biomedicines.

Dr. Stefano Indraccolo
Dr. Paola Ulivi
Guest Editors

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Published Papers (7 papers)

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14 pages, 24365 KiB

Open AccessArticle

MSI Analysis in Solid and Liquid Biopsies of Gastroesophageal Adenocarcinoma Patients: A Molecular Approach

by Elisa Boldrin, Maria Assunta Piano, Rita Alfieri, Marcodomenico Mazza, Loretta Vassallo, Antonio Scapinello, Pierluigi Pilati and Matteo Curtarello

Int. J. Mol. Sci. 2021, 22(14), 7244; https://doi.org/10.3390/ijms22147244 - 6 Jul 2021

Cited by 10 | Viewed by 3768

Abstract

Gastroesophageal adenocarcinoma (GEA) patients with the microsatellite instability (MSI) subtype emerged as optimal candidates for immunotherapy. To date, immunohistochemistry (IHC) is the gold standard for MSI assessment in formalin-fixed paraffin-embedded (FFPE) specimens. However, IHC, although useful for diagnostic typing, cannot be used to analyze cell-free DNA (cfDNA) in liquid biopsy, a tool that could overcome tumor heterogeneity and enable longitudinal monitoring. In order to find an alternative diagnostic method to IHC, we analyzed 86 retrospective GEAs FFPE samples with multiplex PCR. Moreover, to verify the feasibility of MSI detection in liquid biopsy, cfDNA samples of five patients that resulted in having MSI in a prospective cohort of 35 patients were evaluated by multiplex PCR, real-time PCR and droplet digital PCR (ddPCR). Analysis of FFPE showed 100% concordance between multiplex PCR and IHC (Cohen’s Kappa agreement = 1). On the contrary, only ddPCR was able to detect MSI in cfDNAs of T3/T4 GEA patients. In conclusion, data highlight the molecular analysis as an optimal alternative to IHC for the diagnostic typing and suggest that the ddPCR assay can be considered as the most reliable and promising molecular approach to detect MSI in the cfDNA of GEA patients. Full article

(This article belongs to the Special Issue Liquid Biopsies in Cancer Diagnosis, Monitoring and Prognosis)

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Figure 1
Representative IHC staining for MMR proteins and electropherograms of multiplex PCR analysis using the MSI Analysis System Version 1.2 kit. (a) MLH1, MSH2, MSH6 and PSM2 expression in FFPE samples of a MSS and a MSI patient by IHC (original magnification 20×). The MSS patient shows normal expression of all MMR proteins. Deficiency in MLH1 and PSM2 proteins is observed in the MSI patient; (b) Multiplex PCR electropherograms show profiles of 5 quasimonomorphic microsatellites (NR-21, BAT-26, BAT-25, NR-24 and MONO-27) in the normal and tumor tissue of the same patient. The tumor tissue shows additional peaks that are absent in the normal tissue of all microsatellites analyzed, revealing an MSI profile. Full article ">Figure 2
Electropherograms and gel-like image of cfDNA samples analyzed with Agilent TapeStation 2200. The fragments around 35 bps, between 150 and 200 bps and >1000 bps represent the lower marker, the cfDNA and the germline DNA, respectively. Profile of a cfDNA (a) without germline DNA contamination, (b) with minimal and (c) with high contamination; (d) electrophoretic runs of the cfDNA samples of panels (a–c). The percentage of cfDNA is reported below each lane. Full article ">Figure 3
Two-dimensional plot of droplet fluorescence for the three ddPCR MSI assays (BAT-25 and BAT-26; NR-21 and NR-24 and MONO-27) performed in the cfDNA of patients GP06 and GP26. Wild-type molecules are in the orange clusters, and the microsatellite unstable molecules are in the blue clusters. The individual target is labeled on each plot. Circles identify loci with at least three positive droplets (unstable loci). Full article ">Figure 4
MSI status in cfDNA samples of GP06, GP24 and GP26 prospective patients. Black and white rectangles indicate MSI or MSS status, respectively. Unstable microsatellites are shown in red and the number of positive droplets is indicated in brackets. Full article ">

17 pages, 969 KiB

Open AccessArticle

The Physiological MicroRNA Landscape in Nipple Aspirate Fluid: Differences and Similarities with Breast Tissue, Breast Milk, Plasma and Serum

by Susana I. S. Patuleia, Carla H. van Gils, Angie M. Oneto Cao, Marije F. Bakker, Paul J. van Diest, Elsken van der Wall and Cathy B. Moelans

Int. J. Mol. Sci. 2020, 21(22), 8466; https://doi.org/10.3390/ijms21228466 - 11 Nov 2020

Cited by 10 | Viewed by 2524

Abstract

Background: MicroRNAs (miRNAs) target 60% of human messenger RNAs and can be detected in tissues and biofluids without loss of stability during sample processing, making them highly appraised upcoming biomarkers for evaluation of disease. However, reporting of the abundantly expressed miRNAs in healthy samples is often surpassed. Here, we characterized for the first time the physiological miRNA landscape in a biofluid of the healthy breast: nipple aspirate fluid (NAF), and compared NAF miRNA expression patterns with publically available miRNA expression profiles of healthy breast tissue, breast milk, plasma and serum. Methods: MiRNA RT-qPCR profiling of NAF (n = 41) and serum (n = 23) samples from two healthy female cohorts was performed using the TaqMan OpenArray Human Advanced MicroRNA 754-Panel. MiRNA quantification data based on non-targeted or multi-targeted profiling techniques for breast tissue, breast milk, plasma and serum were retrieved from the literature by means of a systematic search. MiRNAs from each individual study were orderly ranked between 1 and 50, combined into an overall ranking per sample type and compared. Results: NAF expressed 11 unique miRNAs and shared 21/50 miRNAs with breast tissue. Seven miRNAs were shared between the five sample types. Overlap between sample types varied between 42% and 62%. Highly ranked NAF miRNAs have established roles in breast carcinogenesis. Conclusion: This is the first study to characterize and compare the unique physiological NAF-derived miRNA landscape with the physiological expression pattern in breast tissue, breast milk, plasma and serum. Breast-specific sources did not mutually overlap more than with systemic sources. Given their established role in carcinogenesis, NAF miRNA assessment could be a valuable tool in breast tumor diagnostics. Full article

(This article belongs to the Special Issue Liquid Biopsies in Cancer Diagnosis, Monitoring and Prognosis)

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18 pages, 6596 KiB

Open AccessArticle

SMAD3 Hypomethylation as a Biomarker for Early Prediction of Colorectal Cancer

by Muhamad Ansar, Chun-Jung Wang, Yu-Han Wang, Tsung-Hua Shen, Chin-Sheng Hung, Shih-Ching Chang and Ruo-Kai Lin

Int. J. Mol. Sci. 2020, 21(19), 7395; https://doi.org/10.3390/ijms21197395 - 7 Oct 2020

Cited by 16 | Viewed by 4554

Abstract

The incidence and mortality rates of colorectal cancer (CRC) have been high in recent years. Prevention and early detection are crucial for decreasing the death rate. Therefore, this study aims to characterize the alteration patterns of mothers against decapentaplegic homolog 3 (SMAD3) in patients with CRC and its applications in early detection by using a genome-wide methylation array to identify an aberrant hypomethylation site in the intron position of the SMAD3 gene. Quantitative methylation-specific polymerase chain reaction showed that hypomethylated SMAD3 occurred in 91.4% (501/548) of Taiwanese CRC tissues and 66.6% of benign tubular adenoma polyps. In addition, SMAD3 hypomethylation was observed in 94.7% of patients with CRC from The Cancer Genome Atlas dataset. A decrease in circulating cell-free methylation SMAD3 was detected in 70% of CRC patients but in only 20% of healthy individuals. SMAD3 mRNA expression was low in 42.9% of Taiwanese CRC tumor tissues but high in 29.4% of tumors compared with paired adjacent normal tissues. Hypomethylated SMAD3 was found in cancers of the digestive system, such as liver cancer, gastric cancer, and colorectal cancer, but not in breast cancer, endometrial cancer, and lung cancer. In conclusion, SMAD3 hypomethylation is a potential diagnostic marker for CRC in Western and Asian populations. Full article

(This article belongs to the Special Issue Liquid Biopsies in Cancer Diagnosis, Monitoring and Prognosis)

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22 pages, 3038 KiB

Open AccessReview

Liquid Biopsies in the Clinical Management of Germ Cell Tumor Patients: State-of-the-Art and Future Directions

by João Lobo, Ricardo Leão, Carmen Jerónimo and Rui Henrique

Int. J. Mol. Sci. 2021, 22(5), 2654; https://doi.org/10.3390/ijms22052654 - 6 Mar 2021

Cited by 17 | Viewed by 3200

Abstract

Liquid biopsies constitute a minimally invasive means of managing cancer patients, entailing early diagnosis, follow-up and prediction of response to therapy. Their use in the germ cell tumor field is invaluable since diagnostic tissue biopsies (which are invasive) are often not performed, and therefore only a presumptive diagnosis can be made, confirmed upon examination of the surgical specimen. Herein, we provide an overall review of the current liquid biopsy-based biomarkers of this disease, including the classical, routinely used serum tumor markers—the promising microRNAs rapidly approaching the introduction into clinical practice—but also cell-free DNA markers (including DNA methylation) and circulating tumor cells. Finally, and importantly, we also explore novel strategies and challenges for liquid biopsy markers and methodologies, providing a critical view of the future directions for liquid biopsy tests in this field, highlighting gaps and unanswered questions. Full article

(This article belongs to the Special Issue Liquid Biopsies in Cancer Diagnosis, Monitoring and Prognosis)

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23 pages, 795 KiB

Open AccessReview

Current Status of Circulating Tumor Cells, Circulating Tumor DNA, and Exosomes in Breast Cancer Liquid Biopsies

by Marta Tellez-Gabriel, Erik Knutsen and Maria Perander

Int. J. Mol. Sci. 2020, 21(24), 9457; https://doi.org/10.3390/ijms21249457 - 11 Dec 2020

Cited by 72 | Viewed by 7465

Abstract

Breast cancer is the most common cancer among women worldwide. Although the five-, ten- and fifteen-year survival rates are good for breast cancer patients diagnosed with early-stage disease, some cancers recur many years after completion of primary therapy. Tumor heterogeneity and clonal evolution may lead to distant metastasis and therapy resistance, which are the main causes of breast cancer-associated deaths. In the clinic today, imaging techniques like mammography and tissue biopsies are used to diagnose breast cancer. Even though these methods are important in primary diagnosis, they have limitations when it comes to longitudinal monitoring of residual disease after treatment, disease progression, therapy responses, and disease recurrence. Over the last few years, there has been an increasing interest in the diagnostic, prognostic, and predictive potential of circulating cancer-derived material acquired through liquid biopsies in breast cancer. Thanks to the development of sensitive devices and platforms, a variety of tumor-derived material, including circulating cancer cells (CTCs), circulating DNA (ctDNA), and biomolecules encapsulated in extracellular vesicles, can now be extracted and analyzed from body fluids. Here we will review the most recent studies on breast cancer, demonstrating the clinical potential and utility of CTCs and ctDNA. We will also review literature illustrating the potential of circulating exosomal RNA and proteins as future biomarkers in breast cancer. Finally, we will discuss some of the advantages and limitations of liquid biopsies and the future perspectives of this field in breast cancer management. Full article

(This article belongs to the Special Issue Liquid Biopsies in Cancer Diagnosis, Monitoring and Prognosis)

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17 pages, 1991 KiB

Open AccessCase Report

Comparative Molecular Analysis of Primary Central Nervous System Lymphomas and Matched Vitreoretinal Lymphomas by Vitreous Liquid Biopsy

by Daniel A. Balikov, Kevin Hu, Chia-Jen Liu, Bryan L. Betz, Arul M. Chinnaiyan, Laxmi V. Devisetty, Sriram Venneti, Scott A. Tomlins, Andi K. Cani and Rajesh C. Rao

Int. J. Mol. Sci. 2021, 22(18), 9992; https://doi.org/10.3390/ijms22189992 - 16 Sep 2021

Cited by 10 | Viewed by 3164

Abstract

Primary Central Nervous System Lymphoma (PCNSL) is a lymphoid malignancy of the brain that occurs in ~1500 patients per year in the US. PCNSL can spread to the vitreous and retina, where it is known as vitreoretinal lymphoma (VRL). While confirmatory testing for diagnosis is dependent on invasive brain tissue or cerebrospinal fluid sampling, the ability to access the vitreous as a proximal biofluid for liquid biopsy to diagnose PCNSL is an attractive prospect given ease of access and minimization of risks and complications from other biopsy strategies. However, the extent to which VRL, previously considered genetically identical to PCNSL, resembles PCNSL in the same individual with respect to genetic alterations, diagnostic strategies, and precision-medicine based approaches has hitherto not been explored. Furthermore, the degree of intra-patient tumor genomic heterogeneity between the brain and vitreous sites has not been studied. In this work, we report on targeted DNA next-generation sequencing (NGS) of matched brain and vitreous samples in two patients who each harbored VRL and PCSNL. Our strategy showed enhanced sensitivity for molecular diagnosis confirmation over current clinically used vitreous liquid biopsy methods. We observed a clonal relationship between the eye and brain samples in both patients, which carried clonal CDKN2A deep deletions, a highly recurrent alteration in VRL patients, as well as MYD88 p.L265P activating mutation in one patient. Several subclonal alterations, however, in the genes SETD2, BRCA2, TERT, and broad chromosomal regions showed heterogeneity between the brain and the eyes, between the two eyes, and among different regions of the PCNSL brain lesion. Taken together, our data show that NGS of vitreous liquid biopsies in PCNSL patients with VRL highlights shared and distinct genetic alterations that suggest a common origin for these lymphomas, but with additional site-specific alterations. Liquid biopsy of VRL accurately replicates the findings for PCNSL truncal (tumor-initiating) genomic alterations; it can also nominate precision medicine interventions and shows intra-patient heterogeneity in subclonal alterations. To the best of our knowledge, this study represents the first interrogation of genetic underpinnings of PCNSL with matched VRL samples. Our findings support continued investigation into the utility of vitreous liquid biopsy in precision diagnosis and treatment of PCNSL/VRL. Full article

(This article belongs to the Special Issue Liquid Biopsies in Cancer Diagnosis, Monitoring and Prognosis)

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Figure 1
Clonality testing in brain and vitreous liquid biopsy lymphoma samples. DNA obtained from brain PCNSL FFPE tissue and vitreous fluid underwent clonal IGH rearrangement PCR testing covering ~90% of the most common rearrangements. Assays were run in duplicate with negative controls (one replicate shown per sample). Assay includes three rearrangement frameworks, 1 (blue), 2 (green), and 3 (red), the colors indicating different fluorophores used to detect the PCR amplicon. Samples containing clonal populations can show rearrangement product (peaks) in one or more frameworks. Clonal rearrangements were defined as peaks identical between replicates that were at least 2× higher than the third highest peak. Capillary electropherogram plots of band intensity over fragment length show a positive PCR result for IGH gene rearrangement in Case 1 (A) but not Case 2 (B). Full article ">Figure 2
Genomic analysis of matched brain tissue and vitreous liquid biopsy samples for Cases 1 and 2. Integrative heatmaps showing genomic alterations detected in Case 1 (A) and Case 2 (B). NGS using the OCPv1 panel was performed on each DNA sample. Gene copy number losses (navy blue for deep and light blue for shallow deletions) and gains (red), as well as gene mutations (green) and short insertions/deletions (indels, brown) with the respective amino acid changes are shown. Numbers inside mutation or indel boxes represent the variant fraction, i.e., fraction of mutated sequencing reads with respect to total reads covering that base. Variant fractions deviate from 0.5 and 1.0 due to normal DNA mixed with the tumor DNA sample. Unfilled boxes represent wild-type status for that position. Full article ">Figure 3
Copy number plots of matched brain tissue and vitreous liquid biopsy samples for Case 1. Copy number plots for each sample are shown as log2 copy number ratio (amplicon-level ratio between read counts in the tumor sample and read counts in a composite of normal samples, normalized for sequencing depth and GC content). Dots represent individual amplicon log 2 copy number ratios. Dots of the same color represent a gene, and black horizontal bars represent average gene-level log2 copy number ratio estimates (coverage-weighted). Genes are listed at the bottom in chromosome order, and chromosomes are separated by gray lines and marked at the top. Genes marked with * have two groups of amplicons with different colors covering them. Altered/relevant genes are highlighted with thick, black gene-level log2 copy number ratio lines. Altered, broad genomic regions are marked with black ovals. Full article ">Figure 4
Copy number plots of matched brain tissue and vitreous liquid biopsy samples for Case 2. Copy number plots for each sample are shown as log2 copy number ratio (amplicon-level ratio between read counts in the tumor sample and read counts in a composite of normal samples, normalized for sequencing depth and GC content). Dots represent individual amplicon log 2 copy number ratios. Dots of the same color represent a gene, and black horizontal bars represent average gene-level log2 copy number ratio estimates (coverage-weighted). Genes are listed at the bottom in chromosome order and chromosomes are separated by gray lines and marked at the top. Genes marked with * have two groups of amplicons with different colors covering them. Altered/relevant genes are highlighted with thick, black lines for gene-level log2 copy number ratios. Full article ">

8 pages, 1241 KiB

Open AccessCase Report

Molecular Characterization of a Rare Case of Bilateral Vitreoretinal T Cell Lymphoma through Vitreous Liquid Biopsy

by Andi K. Cani, Marcus A. Toral, Daniel A. Balikov, Bryan L. Betz, Kevin Hu, Chia-Jen Liu, Matthew V. Prifti, Arul M. Chinnaiyan, Scott A. Tomlins, Vinit B. Mahajan and Rajesh C. Rao

Int. J. Mol. Sci. 2021, 22(11), 6099; https://doi.org/10.3390/ijms22116099 - 5 Jun 2021

Cited by 3 | Viewed by 2705

Abstract

Vitreoretinal lymphoma (VRL) is an uncommon eye malignancy, and VRLs of T cell origin are rare. They are difficult to treat, and their molecular underpinnings, including actionable genomic alterations, remain to be elucidated. At present, vitreous fluid liquid biopsies represent a valuable VRL sample for molecular analysis to study VRLs. In this study, we report the molecular diagnostic workup of a rare case of bilateral T cell VRL and characterize its genomic landscape, including identification of potentially targetable alterations. Using next-generation sequencing of vitreous-derived DNA with a pan-cancer 126-gene panel, we found a copy number gain of BRAF and copy number loss of tumor suppressor DNMT3A. To the best of our knowledge, this represents the first exploration of the T cell VRL cancer genome and supports vitreous liquid biopsy as a suitable approach for precision oncology treatments. Full article

(This article belongs to the Special Issue Liquid Biopsies in Cancer Diagnosis, Monitoring and Prognosis)

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Figure 1
Clinical examination shows vitreous debris in both eyes. (A) Ultra-widefield retinal imaging of the right eye (OD) showed vitreous clumps over the posterior pole. (B) Ultra-widefield retinal imaging of the left eye (OS) showed vitreous cells (black arrowheads); inferior snowballs (white arrowheads); and dense vitreous clumps over the posterior pole. (C,D) Infrared en-face imaging shows level (green-line) at which optical coherence tomography (OCT) was used to image cross-section of macula (E,F). Cross-sectional OCT showed (C) mild epiretinal membrane OD and (D) a dense vitreous opacity over the macula OS. Posterior B-Scan ultrasonography revealed vitreous opacities (G) OD and (H) OS. (I) Cytological examination for morphology and cell-surface marker staining for CD20, CD10 and CD3 as well as vitreous DNA amounts are shown for each vitreous sample. Full article ">Figure 2
DNA analysis of vitreous liquid biopsy samples. (A) DNA obtained from vitreous fluid from each eye underwent clonal T cell receptor (TCR) rearrangement PCR testing covering ~90% of the most common rearrangements in the TCRB and TCRG genes. Assays were run in duplicate with negative controls (one replicate shown per sample). Clonal rearrangements were defined as peaks identical between replicates that were at least 2× higher than the third highest peak. Capillary electropherogram plots of band intensity over fragment length show a positive PCR result for TCRG rearrangement at 186 bp, identical in both eyes, at ~10% frequency. No TCRB-positive bands were observed in either sample. (B) NGS using the OCP version 1 panel was performed on each eye sample. Copy number plots are shown as log2 copy number ratio (amplicon level ratio between read counts in the tumor sample and read counts in a composite of normal samples, normalized for sequencing depth and GC content). Dots represent individual amplicons, dots of the same color represent a gene, and black horizontal bars represent average gene-level estimates (coverage-weighted). Altered/relevant genes are highlighted. No mutations were observed in either sample. Full article ">

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