TABLE 1.
Studies identifying the dependence of cell migration on heterochromatin levels.
| Heterochromatin alteration and the effect on migration | Cell type (*-primary cells) | Method of manipulation | Migration assay | References |
| H3K27me3 reduction leading to inhibition of migration | Bone marrow-derived mesenchymal stem cells* | EZH2 siRNA | TA | Liu et al., 2018 |
| Mouse embryonic fibroblasts* | EZH2 siRNA | TA and WH | Kottakis et al., 2011 | |
| Endometriotic epithelial cells | EZH2 siRNA and inhibitor (GSK126) | TA and WH | Eskander et al., 2013; Zhang et al., 2017 | |
| Squamous cell carcinoma | EZH2 siRNA and inhibitors (GSK126 and EPZ-6438) | WH | Adhikary et al., 2015 | |
| Immortalized keratinocytes | EZH2 siRNA | WH | Adhikary et al., 2015 | |
| Melanoma | EZH2 siRNA and inhibitors (GSK126 and GSK343) | TA and WH | Luo et al., 2013; Maizels et al., 2017 | |
| Pancreatic cancer cells | EZH2 siRNA | TA and WH | Ma et al., 2018 | |
| Ovarian cancer cells | EZH2 siRNA | TA | Lu et al., 2010; Rao et al., 2010 | |
| Breast carcinoma cells | EZH2 siRNA | TA | Varambally et al., 2008 | |
| Prostate cancer cells | EZH2 siRNA | WH | Varambally et al., 2008 | |
| H3K27me3 enhancement leading to acceleration of migration | Pancreatic cancer cells | EZH2 OE | TA and WH | Ma et al., 2018 |
| H3K9me2/3 reduction leading to inhibition of migration | Vascular smooth muscle cells* | SUV39H1 siRNA | TA | Zhang et al., 2019a |
| Melanoma cells | SUV39H1/2 inhibitor (chaetocin) and SETDB1 siRNA | TA and WH | Gerlitz and Bustin, 2010; Maizels et al., 2017; Orouji et al., 2019 | |
| Liver cancer cells | SETDB1 siRNA | TA | Wong et al., 2016; Zhang et al., 2018 | |
| Gastric cancer cells | SETDB1 siRNA | TA | Nishikawaji et al., 2016 | |
| Lymphocytes | G9a siRNA and inhibitor (BIX01294) | TA and Collagen matrix assay | Zhang X. et al., 2016; Madrazo et al., 2018 | |
| Glioma cells | SETDB1 and SUV39H1 siRNA, SUV39H1/2 inhibitor (chaetocin) | WH | Spyropoulou et al., 2014; Sepsa et al., 2015 | |
| Breast cancer cells | SUV39H1 siRNA and SUV39H1/2 inhibitor (chaetocin) | TA and WH | Yokoyama et al., 2013 | |
| Cervical cancer cells | G9a inhibitor (BIX01294) | TA and WH | Chen et al., 2017 | |
| Lung cancer cells | G9a siRNA, inhibitor (BIX01294) and DN | TA and WH | Chen et al., 2010; Huang et al., 2017 | |
| Colon cancer cells | SETDB1 siRNA | TA | Yu et al., 2019 | |
| Melanoma cells | SUV39H1/2 inhibitor (chaetocin) | TA and WH | Gerlitz and Bustin, 2010; Maizels et al., 2017 | |
| H3K9me2/3 enhancement leading to acceleration of migration | Vascular smooth muscle cells* | SUV39H1 OE | TA | Zhang et al., 2019a |
| Melanoma cells | SETDB1 OE | TA and WH | Orouji et al., 2019 | |
| Liver cancer cells | SETDB1 OE | TA | Zhang et al., 2018 | |
| Gastric cancer cells | SETDB1 OE | TA | Nishikawaji et al., 2016 | |
| Breast cancer cells | SUV39H1 OE | TA | Yokoyama et al., 2013 | |
| Lung cancer cells | G9a OE | TA | Chen et al., 2010 | |
| Colon cancer cells | SETDB1 OE | TA | Yu et al., 2019 | |
| Reduction in DNA methylation leading to inhibition of migration | Cortical interneurons* | DNMT1 KO | Organotypic brain slice culture | Pensold et al., 2017 |
| Corneal epithelial cells* | DNMT1 siRNA | WH | Luo et al., 2019 | |
| Breast cancer cells | DNMT inhibitors (AZA, SGI, C02S) | TA and WH | Shafiei et al., 2008; Su et al., 2018; Yuan et al., 2019 | |
| Prostate cancer cells | DNMT inhibitor (AZA) | WH | Strmiska et al., 2019 | |
| Ovarian cancer cells | DNMT inhibitor (AZA) | TA | Meng et al., 2013 | |
| Lung cancer cells | DNMT1, 3a siRNA, DNMT inhibitor (AZA) | TA and WH | Mateen et al., 2013; Yan et al., 2014; Bu et al., 2018 | |
| Glioma cells | DNMT3a,b siRNA, DNMT inhibitor (AZA) | TA and WH | Wang et al., 2015; Xu et al., 2015; Guo et al., 2017 | |
| Esophageal cancer cells | DNMT inhibitor (AZA) | WH | Ahrens et al., 2015 | |
| Osteosarcoma cells | DNMT inhibitor (AZA) | WH | Gong et al., 2019 | |
| Pancreatic cancer cells | DNMT3b siRNA | TA and WH | Wang et al., 2019 | |
| Colon cancer cells | DNMT inhibitor (AZA) | WH | Oshima et al., 2019 | |
| Trophoblasts | DNMT inhibitor (AZA) | TA | Rahnama et al., 2006 | |
| DNA methylation enhancement leading to acceleration of migration | Lung cancer cells | DNMT3a OE | WH | Yan et al., 2014 |
| Liver cancer cells | DNMT3b OE | WH | Wu et al., 2019 | |
| Histone acetylation elevation leading to inhibition of migration | Bone marrow-derived mesenchymal stem cells* | HDAC inhibitor (TSA) | TA | Liu et al., 2018 |
| Neurons in C. elegans development* | HDAC1 mutations and HDAC inhibitor (TSA) | Whole animal development | Zinovyeva et al., 2006; Nambiar et al., 2007 | |
| Schwann cells* | HDAC inhibitor (TSA) | TA | Wang et al., 2014 | |
| Endothelial cells* | HDAC7 siRNA | WH | Mottet et al., 2007 | |
| Smooth muscle cells* | HDAC4 siRNA and HDAC inhibitor (TSA) | TA | Yang et al., 2012; Usui et al., 2014 | |
| Cardiac fibroblasts* | HDAC1 inhibition (ellagic acid) | TA | Lin et al., 2019 | |
| Dendritic cells* | HDAC inhibitor (TSA) | TA | Kim et al., 2013 | |
| Tenocytes* | HDAC inhibitor (TSA) | WH | Zhang B. et al., 2016 | |
| Melanoma cells | HDAC inhibitor (TSA) | TA and WH | Gerlitz and Bustin, 2010 | |
| Breast cancer cells | HDAC2, 5, 8 siRNA, HDAC inhibitors (MS275, SB939, LBH, Tub, C02S, PCI-34051, VPA) | TA and WH | Jeon and Lee, 2010; Zhang et al., 2012; Hsieh et al., 2016; Li et al., 2016; Su et al., 2018; Yuan et al., 2019 | |
| Ovarian cancer cells | HDAC3, 4 siRNA, HDAC inhibitor (TSA) | TA | Hayashi et al., 2010; Ahn et al., 2012; Meng et al., 2013 | |
| Lung cancer cells | HDAC inhibitor (Silibinin) | TA | Mateen et al., 2013 | |
| Esophageal cancer cells | HDAC inhibitor (MS-275) | WH | Ahrens et al., 2015 | |
| Transformed macrophages | HDAC inhibitor (Butyrate) | TA | Maa et al., 2010 | |
| Oral cancer cells | HDAC2 siRNA | WH | Chang et al., 2011 | |
| Prostate cancer cells | HDAC inhibitor (VPA) | TA | Wedel et al., 2011 | |
| Glioma cells | HDAC3 siRNA | TA and WH | Zhu et al., 2013 | |
| Broad histone methylation inhibition leading to chromatin decondensation and inhibition of migration | Bone marrow-derived mesenchymal stem cells* | DZNep | TA | Liu et al., 2018 |
| Tenocytes* | MTA | WH | Zhang B. et al., 2016 | |
| Chondrosarcoma | DZNep | WH | Girard et al., 2014 | |
| Melanoma cells | MTA | TA and WH | Gerlitz and Bustin, 2010 | |
| Histone H1 alterations leading to inhibition of migration | Melanoma cells | OE of histone H1 DN | TA | Gerlitz et al., 2007 |
| Glioma, osteosarcoma and gastric cancer cells | OE of histone H1 DN | TA | Sang et al., 2019; Zhang et al., 2019b; Xu et al., 2020 |
OE, over expression; DN, over expression of a dominant negative form; TA, transwell assay; WH, wound healing assay; SGI, Guadecitabine/SGI-110; MS275, Entinostat; Tub, Tubastatin A HCL; TSA, Trichostatin A; VPA, Valproic acid; DZNep, 3-Deazaneplanocin-A; MTA, 5′-deoxy-5′-methylthioadenosine.