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

Deadline for manuscript submissions: closed (31 January 2023) | Viewed by 29722

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Dr. Antonio Simone Laganà

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Department of Obstetrics and Gynecology, “Filippo Del Ponte” Hospital, University of Insubria, 21100 Varese, VA, Italy
Interests: women’s health; minimally invasive procedures; up-to-date management; gynecology; reproductive health; surgery
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Dear Colleagues,

Endometriosis is defined as the presence of endometrial-like endometrial cells, glands, and stroma outside the uterus, causing a strong inflammatory-like microenvironment in the affected tissue. The exact prevalence of endometriosis is unknown, but estimates range from 2%–10% of women of reproductive age to 50% of infertile women. The etiopathogenesis of endometriosis remains controversial—immune, hormonal, genetic, and epigenetic factors may all be involved, and several theories have been proposed to explain it.

This Special Issue aims to publish groundbreaking research and review articles in basic and translational science (immunology, cell biology, genetics, and epigenetics) that may create new scenarios and change our perspective of the topic.

Dr. Antonio Simone Laganà
Guest Editor

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Keywords

endometriosis
reproductive immunology
inflammation
cytokines
infertility
in vitro fertilization
peritoneal fluid
apoptosis
epigenetics
ovary

Related Special Issues

Endometriosis Research: From Bench to Bedside in International Journal of Molecular Sciences (7 articles)
Molecular and Cellular Advances in Endometriosis Research in International Journal of Molecular Sciences (14 articles)
Endometriosis: Focusing on Molecular and Cellular Research in International Journal of Molecular Sciences (5 articles)
Molecular and Cellular Advances in Endometriosis Research 3.0 in International Journal of Molecular Sciences (2 articles)

Published Papers (12 papers)

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Editorial

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3 pages, 216 KiB

Open AccessEditorial

Molecular and Cellular Advances in Endometriosis Research: Paving the Way for Future Directions

by Antonio Simone Laganà, Federico Ferrari, Donatella Mangione, Fabio Fiorino, Alessandra Vassiliadis and Renato Venezia

Int. J. Mol. Sci. 2023, 24(16), 12663; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms241612663 - 11 Aug 2023

Viewed by 838

Abstract

Molecular and cellular research in the field of endometriosis is moving forward in giant steps [...] Full article

(This article belongs to the Special Issue Molecular and Cellular Advances in Endometriosis Research 2.0)

Research

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14 pages, 1136 KiB

Open AccessArticle

Altered Differential Expression of Genes and microRNAs Related to Adhesion and Apoptosis Pathways in Patients with Different Phenotypes of Endometriosis

by Luana Grupioni Lourenço Antonio, Juliana Meola, Ana Carolina Japur de Sá Rosa-e-Silva, Antonio Alberto Nogueira, Francisco José Candido dos Reis, Omero Benedicto Poli-Neto and Julio César Rosa-e-Silva

Int. J. Mol. Sci. 2023, 24(5), 4434; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24054434 - 23 Feb 2023

Cited by 4 | Viewed by 1266

Abstract

We aim to investigate the expression of genes (MAPK1 and CAPN2) and microRNAs (miR-30a-5p, miR-7-5p, miR-143-3p, and miR-93-5p) involved in adhesion and apoptosis pathways in superficial peritoneal endometriosis (SE), deep infiltrating endometriosis (DE), and ovarian endometrioma (OE), and to evaluate whether these lesions share the same pathophysiological mechanisms. We used samples of SE (n = 10), DE (n = 10), and OE (n = 10), and endometrial biopsies of these respective patients affected with endometriosis under treatment at a tertiary University Hospital. Endometrial biopsies collected in the tubal ligation procedure from women without endometriosis comprised the control group (n = 10). Quantitative real-time polymerase chain reaction was performed. The expression of MAPK1 (p < 0.0001), miR-93-5p (p = 0.0168), and miR-7-5p (p = 0.0006) was significantly lower in the SE group than in the DE and OE groups. The expression of miR-30a (p = 0.0018) and miR-93 (p = 0.0052) was significantly upregulated in the eutopic endometrium of women with endometriosis compared to the controls. MiR-143 (p = 0.0225) expression also showed a statistical difference between the eutopic endometrium of women with endometriosis and the control group. In summary, SE showed lower pro-survival gene expression and miRNAs involved in this pathway, indicating that this phenotype has a different pathophysiological mechanism compared to DE and OE. Full article

(This article belongs to the Special Issue Molecular and Cellular Advances in Endometriosis Research 2.0)

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13 pages, 1266 KiB

Open AccessArticle

Plasma and Peritoneal Fluid Fibronectin and Collagen IV Levels as Potential Biomarkers of Endometriosis

by Damian Warzecha, Julia Załęcka, Grzegorz Mańka, Mariusz Kiecka, Michał Lipa, Robert Spaczyński, Piotr Piekarski, Beata Banaszewska, Artur Jakimiuk, Tadeusz Issat, Wojciech Rokita, Jakub Młodawski, Maria Szubert, Piotr Sieroszewski, Grzegorz Raba, Kamil Szczupak, Tomasz Kluz, Marek Kluza, Mirosław Wielgoś, Łukasz Ołdak, Anna Leśniewska, Ewa Gorodkiewicz and Piotr Laudański Show full author list Hide full author list

Int. J. Mol. Sci. 2022, 23(24), 15669; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms232415669 - 10 Dec 2022

Cited by 4 | Viewed by 1340

Abstract

Laparoscopy as a diagnostic tool for patients with suspected endometriosis is associated with several potentially life-threatening complications. Therefore, it is imperative to identify reliable, non-invasive biomarkers of the disease. The aim of this study was to analyse the concentrations of fibronectin and type IV collagen in peritoneal fluid and plasma to assess their role as potential biomarkers in the diagnosis of endometriosis. Fibronectin and collagen IV protein levels were assessed by surface plasmon resonance imaging (SPRi) biosensors with the usage of monoclonal antibodies. All patients enrolled in the study were referred for laparoscopy for the diagnosis of infertility or chronic pelvic pain (n = 84). The study group included patients with endometriosis confirmed during surgery (n = 49). The concentration of fibronectin in the plasma (329.3 ± 98.5 mg/L) and peritoneal fluid (26.8 ± 11.1 μg/L) in women with endometriosis was significantly higher than in the control group (251.2 ± 84.0 mg/L, 7.0 ± 5.9 μg/L). Fibronectin levels were independent of endometriosis stage (p = 0.874, p = 0.469). No significant differences were observed in collagen IV levels (p = 0.385, p = 0.465). The presence of elevated levels of fibronectin may indicate abnormalities in cell–ECM signalling during the course of endometriosis, and may be a potential biomarker for early detection. Full article

(This article belongs to the Special Issue Molecular and Cellular Advances in Endometriosis Research 2.0)

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19 pages, 1450 KiB

Open AccessArticle

Sex Hormone Candidate Gene Polymorphisms Are Associated with Endometriosis

by Ilya Golovchenko, Boris Aizikovich, Oleg Golovchenko, Evgeny Reshetnikov, Maria Churnosova, Inna Aristova, Irina Ponomarenko and Mikhail Churnosov

Int. J. Mol. Sci. 2022, 23(22), 13691; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms232213691 - 08 Nov 2022

Cited by 13 | Viewed by 1682

Abstract

The present study was designed to examine whether sex hormone polymorphisms proven by GWAS are associated with endometriosis risk. Unrelated female participants totaling 1376 in number (395 endometriosis patients and 981 controls) were recruited into the study. Nine single-nucleotide polymorphisms (SNPs) which GWAS correlated with circulating levels of sex hormones were genotyped using a TaqMan allelic discrimination assay. FSH-lowering, and LH- and testosterone-heightening polymorphisms of the FSHB promoter (allelic variants A rs11031002 and C rs11031005) exhibit a protective effect for endometriosis (OR = 0.60–0.68). By contrast, the TT haplotype loci that were GWAS correlated with higher FSH levels and lower LH and testosterone concentrations determined an increased risk for endometriosis (OR = 2.03). Endometriosis-involved epistatic interactions were found between eight loci of sex hormone genes (without rs148982377 ZNF789) within twelve genetic simulation models. In silico examination established that 8 disorder-related loci and 80 proxy SNPs are genome variants affecting the expression, splicing, epigenetic and amino acid conformation of the 34 genes which enrich the organic anion transport and secondary carrier transporter pathways. In conclusion, the present study showed that sex hormone polymorphisms proven by GWAS are associated with endometriosis risk and involved in the molecular pathophysiology of the disease due to their functionality. Full article

(This article belongs to the Special Issue Molecular and Cellular Advances in Endometriosis Research 2.0)

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18 pages, 6111 KiB

Open AccessArticle

Clinical Value of the PD-1/PD-L1/PD-L2 Pathway in Patients Suffering from Endometriosis

by Dorota Suszczyk, Wiktoria Skiba, Witold Zardzewiały, Anna Pawłowska, Karolina Włodarczyk, Grzegorz Polak, Rafał Tarkowski and Iwona Wertel

Int. J. Mol. Sci. 2022, 23(19), 11607; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms231911607 - 01 Oct 2022

Cited by 4 | Viewed by 2111

Abstract

The interaction between dendritic cells (DCs) and T cells mediated by the programmed cell death 1 (PD-1)/programmed cell death ligand 1 (PD-L1)/programmed cell death ligand 2 (PD-L2) pathway is the most important point in regulating immunological tolerance and autoimmunity. Disturbances in the quantity, maturity, and activity of DCs may be involved in the implantation and growth of endometrial tissue outside the uterus in endometriosis (EMS). However, little is known about the role of the immune checkpoint pathways in EMS. In our study, we examined the expression of PD-L1/PD-L2 on myeloid DCs (mDCs) and plasmacytoid DCs (pDCs) in the peripheral blood (PB) and peritoneal fluid (PF) of both EMS patients (n = 72) and healthy subjects (n = 20) via flow cytometry. The concentration of soluble PD-L1 and PD-L2 in the plasma and PF of EMS patients and the control group were determined using ELISA. We demonstrated an elevated percentage of mDCs, mDCs and pDCs with the PD-L1or PD-L2 expression, and a higher concentration of the soluble forms of PD-L1 and PD-L2 in the PF than in the plasma of EMS patients. We conclude that the peritoneal cavity environment and the PD-1/PD-L1/PD-L2 axis may play an important role in the modulation of immune response and the development and/or progression of EMS. Full article

(This article belongs to the Special Issue Molecular and Cellular Advances in Endometriosis Research 2.0)

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17 pages, 13834 KiB

Open AccessArticle

What Do the Transcriptome and Proteome of Menstrual Blood-Derived Mesenchymal Stem Cells Tell Us about Endometriosis?

by Letícia B. C. Penariol, Carolina H. Thomé, Patrícia A. Tozetti, Carlos R. K. Paier, Fabiana O. Buono, Kamila C. Peronni, Maristela D. Orellana, Dimas T. Covas, Maria E. A. Moraes, Wilson A. Silva, Jr., Júlio C. Rosa-e-Silva, Rui A. Ferriani, Vitor M. Faça, Omero B. Poli-Neto, Daniel G. Tiezzi and Juliana Meola

Int. J. Mol. Sci. 2022, 23(19), 11515; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms231911515 - 29 Sep 2022

Cited by 7 | Viewed by 2771

Abstract

Given the importance of menstrual blood in the pathogenesis of endometriosis and the multifunctional roles of menstrual mesenchymal stem cells (MenSCs) in regenerative medicine, this issue has gained prominence in the scientific community. Moreover, recent reviews highlight how robust the integrated assessment of omics data are for endometriosis. To our knowledge, no study has applied the multi-omics approaches to endometriosis MenSCs. This is a case-control study at a university-affiliated hospital. MenSCs transcriptome and proteome data were obtained by RNA-seq and UHPLC-MS/MS detection. Among the differentially expressed proteins and genes, we emphasize ATF3, ID1, ID3, FOSB, SNAI1, NR4A1, EGR1, LAMC3, and ZFP36 genes and MT2A, TYMP, COL1A1, COL6A2, and NID2 proteins that were already reported in the endometriosis. Our functional enrichment analysis reveals integrated modulating signaling pathways such as epithelial–mesenchymal transition (↑) and PI3K signaling via AKT to mTORC1 (↓ in proteome), mTORC1 signaling, TGF beta signaling, TNFA signaling via NFkB, IL6 STAT3 signaling, and response to hypoxia via HIF1A targets (↑ in transcriptome). Our findings highlight primary changes in the endometriosis MenSCs, suggesting that the chronic inflammatory endometrial microenvironment can modulate these cells, providing opportunities for endometriosis etiopathogenesis. Moreover, they identify challenges for future research leveraging knowledge for regenerative and precision medicine in endometriosis. Full article

(This article belongs to the Special Issue Molecular and Cellular Advances in Endometriosis Research 2.0)

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8 pages, 1672 KiB

Open AccessArticle

The Levels of Ghrelin, Glucagon, Visfatin and Glp-1 Are Decreased in the Peritoneal Fluid of Women with Endometriosis along with the Increased Expression of the CD10 Protease by the Macrophages

by Aleksey M. Krasnyi, Alsu A. Sadekova, Tatyana Y. Smolnova, Vyacheslav V. Chursin, Natalya A. Buralkina, Vladimir D. Chuprynin, Ekaterina Yarotskaya, Stanislav V. Pavlovich and Gennadiy T. Sukhikh

Int. J. Mol. Sci. 2022, 23(18), 10361; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms231810361 - 08 Sep 2022

Cited by 4 | Viewed by 1507

Abstract

The aim of this study was to evaluate the levels of ten energy metabolism factors: C-peptide, ghrelin, GIP, GLP-1, glucagon, insulin, leptin, PAI-1 (total), resistin, and visfatin, and to determine the expression of GLP1R receptors, CD10, CD26 proteases, and pro-inflammatory marker CD86 by macrophages in the peritoneal fluid (PF) in patients with endometriosis. The study included 54 women with endometriosis and a control group of 30 women with uterine myoma without signs of endometriosis. The levels of factors in PF were assessed by a multiplex method. Expression of GLP1R receptors, CD10, CD26 proteases, and CD86 by macrophages was evaluated using flow cytometry. It was found that in women with endometriosis, the concentrations of ghrelin, GLP-1, glucagon, and visfatin in PF were reduced (p = 0.007, p = 0.009, p = 0.002, p = 0.008, respectively). At the same time, there was a noted increase in the CD10 protease expression by peritoneal macrophages (p = 0.044). Correlation analysis showed a positive correlation of ghrelin and GLP-1 levels with CD86 macrophage expression (p = 0.044, p = 0.022, respectively) in the study group; a positive correlation was also found between the levels of GLP-1, glucagon, and visfatin with CD26 macrophage expression (p = 0.041, p = 0.048, p = 0.015, respectively) in PF. No correlations were found in the control group. These results indicate that a decrease in the levels of ghrelin, GLP-1, glucagon, and visfatin in PF may contribute to endometriosis development through their impact on the expression of pro-inflammatory markers of PF macrophages. Full article

(This article belongs to the Special Issue Molecular and Cellular Advances in Endometriosis Research 2.0)

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24 pages, 8453 KiB

Open AccessArticle

Specific Local Predictors That Reflect the Tropism of Endometriosis—A Multiple Immunohistochemistry Technique

by Anca-Maria Istrate-Ofiţeru, Elena-Iuliana-Anamaria Berbecaru, George-Lucian Zorilă, Gabriela-Camelia Roşu, Laurențiu Mihai Dîră, Cristina Maria Comănescu, Roxana Cristina Drăguşin, Dan Ruican, Rodica Daniela Nagy, Dominic Gabriel Iliescu, Laurențiu Mogoantă and Daniel Pirici

Int. J. Mol. Sci. 2022, 23(10), 5614; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23105614 - 17 May 2022

Cited by 2 | Viewed by 3924

Abstract

Ectopic endometrial epithelium associates a wide spectrum of symptomatology. Their evolution can be influenced by inflammatory and vascular changes, that affect not only the structure and cell proliferation rate, but also symptoms. This prospective study involved tissue samples from surgically treated patients, stained using classical histotechniques and immunohistochemistry. We assessed ectopic endometrial glands (CK7+, CK20−), adjacent blood vessels (CD34+), estrogen/progesterone hormone receptors (ER+, PR+), inflammatory cells (CD3+, CD20+, CD68+, Tryptase+), rate of inflammatory cells (Ki67+) and oncoproteins (BCL2+, PTEN+, p53+) involved in the development of endometriosis/adenomyosis. A CK7+/CK20− expression profile was present in the ectopic epithelium and differentiated it from digestive metastases. ER+/PR+ were present in all cases analyzed. We found an increased vascularity (CD34+) in the areas with abdominal endometriosis and CD3+−:T-lymphocytes, CD20+−:B-lymphocytes, CD68+:macrophages, and Tryptase+: mastocytes were abundant, especially in cases with adenomyosis as a marker of proinflammatory microenvironment. In addition, we found a significantly higher division index-(Ki67+) in the areas with adenomyosis, and inactivation of tumor suppressor genes-p53+ in areas with neoplastic changes. The inflammatory/vascular/hormonal mechanisms trigger endometriosis progression and neoplastic changes increasing local pain. Furthermore, they may represent future therapeutic targets. Simultaneous-multiple immunohistochemical labelling represents a valuable technique for rapidly detecting cellular features that facilitate comparative analysis of the studied predictors. Full article

(This article belongs to the Special Issue Molecular and Cellular Advances in Endometriosis Research 2.0)

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Review

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14 pages, 1895 KiB

Open AccessReview

Progesterone Resistance in Endometriosis: Current Evidence and Putative Mechanisms

by Ping Zhang and Guoyun Wang

Int. J. Mol. Sci. 2023, 24(8), 6992; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24086992 - 10 Apr 2023

Cited by 9 | Viewed by 5324

Abstract

Endometriosis is an estrogen-dependent disease characterized by the growth of endometrial-like tissue outside the uterus. Progestins are currently the most commonly used treatment for endometriosis because of their excellent therapeutic effects and limited side effects. However, progestins have been unsuccessful in some symptomatic patients. The inability of the endometrium to respond properly to progesterone is known as progesterone resistance. An increasing body of evidence suggests the loss of progesterone signaling and the existence of progesterone resistance in endometriosis. The mechanisms of progesterone resistance have received considerable scholarly attention in recent years. Abnormal PGR signaling, chronic inflammation, aberrant gene expression, epigenetic alterations, and environmental toxins are considered potential molecular causes of progesterone resistance in endometriosis. The general objective of this review was to summarize the evidence and mechanisms of progesterone resistance. A deeper understanding of how these mechanisms contribute to progesterone resistance may help develop a novel therapeutic regimen for women with endometriosis by reversing progesterone resistance. Full article

(This article belongs to the Special Issue Molecular and Cellular Advances in Endometriosis Research 2.0)

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17 pages, 697 KiB

Open AccessReview

Liquid Biopsy in Endometriosis: A Systematic Review

by Carlo Ronsini, Pietro Fumiento, Irene Iavarone, Pier Francesco Greco, Luigi Cobellis and Pasquale De Franciscis

Int. J. Mol. Sci. 2023, 24(7), 6116; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24076116 - 24 Mar 2023

Cited by 10 | Viewed by 2116

Abstract

Despite laparoscopy being a standardized option to diagnose pelvic endometriotic implants, non-invasive biomarkers are necessary to avoid the discomfort of invasive procedures. Recent evidence suggests a potential role of microRNAs (miRNAs) as feasible biomarkers for the early diagnosis of endometriosis. Following the recommendations in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement, we systematically searched PubMed, EMBASE, Scopus, Cochrane Library, and Science Direct in January 2023. We provided no restriction on the country and year of publication, and considered English published articles. We selected studies including patients with endometriosis and describing miRNA regulation in the context of endometriosis. Overall, 45 studies fulfilled the inclusion criteria, and 2045 patients with endometriosis and 1587 controls were screened. Patients were analyzed concerning miRNAs expression and sources, stage of disease, and symptoms, and compared to controls. Among DEMs, the ones with the widest delta between endometriosis patients and controls—Relative Expression ≥ 4 Log2(ratio)—were miR-145, miR-191, miR-195, miR-21-5p, miR-106b-5p, miR-195-5p, miR-451a, miR-200c, miR-20a-5p, and miR-15a-5p. Although the epigenetic regulation is partially unclear, miRNAs are valid biomarkers to diagnose endometriotic lesions in symptomatic and non-symptomatic women. MiRNAs modulation should be clarified, especially during therapies or relapse, to plan targeted management protocols. Full article

(This article belongs to the Special Issue Molecular and Cellular Advances in Endometriosis Research 2.0)

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14 pages, 3540 KiB

Open AccessReview

Endometriosis and COVID-19: A Systematic Review and Meta-Analysis

by Ziyaana Kabani, Maria E. Ramos-Nino and Prakash V. A. K. Ramdass

Int. J. Mol. Sci. 2022, 23(21), 12951; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms232112951 - 26 Oct 2022

Cited by 11 | Viewed by 3690

Abstract

Endometriosis is defined as ectopic endometrial tissues dispersed outside the endometrium. This can cause disruption in hormonal and immunological processes, which may increase susceptibility to SARS-CoV-2 infection. Worsening of endometriosis symptoms may occur as a result of this infection. The aim of our review was to estimate the pooled prevalence of SARS-CoV-2 infection and the health impacts of the COVID-19 pandemic in endometriosis patients. We conducted a systematic review and meta-analysis. MEDLINE, Science Direct, Scopus, and Google Scholar databases were searched, using the keywords: (endometriosis) AND (COVID-19 OR SARS-CoV-2). Forest plots and pooled estimates were created using the Open Meta Analyst software. After screening 474 articles, 19 studies met the eligibility criteria for the systematic review, and 15 studies were included in the meta-analyses. A total of 17,799 patients were analyzed. The pooled prevalence of SARS-CoV-2 infection in endometriosis patients was 7.5%. Pooled estimates for the health impacts were 47.2% for decreased access to medical care, 49.3% increase in dysmenorrhea, 75% increase in anxiety, 59.4% increase in depression, and 68.9% increase in fatigue. Endometriosis patients were undeniably impacted by the COVID-19 pandemic, which caused the worsening of symptoms such as dysmenorrhea, pelvic pain, anxiety, depression, and fatigue. Full article

(This article belongs to the Special Issue Molecular and Cellular Advances in Endometriosis Research 2.0)

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Other

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9 pages, 1957 KiB

Open AccessCase Report

Endometriosis of the Cervix: A Rare Clinical Case with the Possibility of Comparing the Eutopic and Ectopic Endometrium at the Cellular Level

by Konstantin A. Toniyan, Elena Yu. Gorbacheva, Valery V. Boyarintsev and Irina V. Ogneva

Int. J. Mol. Sci. 2023, 24(3), 2184; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24032184 - 22 Jan 2023

Cited by 2 | Viewed by 1293

Abstract

Endometriosis of the cervix is a rare form of genital endometriosis, which is characterized by the appearance of tissue on the vaginal part of the cervix, similar to the tissue of the mucous membrane of the uterine cavity. We describe a clinical case in which we compared the content of cytoskeletal proteins, H3 histone modifications and DNA methylation (total and 5-hydroxymethylcytosine content) in the eutopic endometrium and in tissue from endometriosis foci on the cervix. The patient had elevated levels of estradiol, interleukin-1β and interleukin-8. At the cellular level, the content of tubulin and the marker of stable microtubules were reduced in the ectopic endometrium (by 45% and 37%, p < 0.05, respectively), but the alpha-actinin-1 content was increased (by 75%, p < 0.05) with an increase in the expression of its gene. At the same time, the total level of DNA methylation in the endometriotic focus was reduced by more than 2 times with the accumulation of the intermediate product 5-hydroxymethylcytosine (the content increased by more than 3 times), probably due to an increase in the content of tet methylcytosine dioxygenase 1 (more than 4 times). Full article

(This article belongs to the Special Issue Molecular and Cellular Advances in Endometriosis Research 2.0)

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