Comparative analysis of milk microRNA in the therian lineage highlights the evolution of lactation
Christophe Lefèvre A B C D , Pooja Venkat B C D , Amit Kumar D , Vengamanaidu Modepalli A and Kevin R. Nicholas
E F G
+ Author Affiliations
- Author Affiliations
A School of Medicine, Deakin University, Pigdons Road, Geelong, Vic. 3220, Australia.
B Division of Bioinformatics, Walter and Eliza Hall Institute of Medical Research, Melbourne, Vic. 3052, Australia.
C Faculty of Medicine, Dentistry and Health Sciences, The University of Melbourne, Vic. 3010, Australia.
D Peter MacCallum Cancer Centre, Melbourne, Vic. 3000, Australia.
E School of Biosciences, The University of Melbourne, Vic. 3010, Australia.
F Department of Drug Delivery, Disposition and Dynamics, Faculty of Pharmacy and Pharmaceutical Sciences, Monash University, 381 Royal Parade, Parkville, Vic. 3052, Australia.
G Corresponding author. Email: kevin.nicholas@monash.edu
Reproduction, Fertility and Development 31(7) 1266-1275 https://doi.org/10.1071/RD18199
Submitted: 11 July 2018 Accepted: 13 March 2019 Published: 24 April 2019
Abstract
Milk is a complex secretion that has an important role in mammalian reproduction. It is only recently that sequencing technologies have allowed the identification and quantification of microRNA (miRNA) in milk of a growing number of mammalian species. This provides a novel window on the study of the evolution and functionality of milk through the comparative analysis of milk miRNA content. Here, milk miRNA sequencing data from five species (one marsupial (tammar wallaby) and four eutherians (human, mouse, cow and pig)) have been retrieved from public depositories and integrated in order to perform a comparison of milk miRNA profiles. The study shows that milk miRNA composition varies widely between species, except for a few miRNAs that are ubiquitously expressed in the milk of all mammals and indicates that milk miRNA secretion has broadly evolved during mammalian evolution. The putative functions of the most abundant milk miRNAs are also discussed.
Additional keywords: evolution, lactation, mammals, milk, miRNA.
References
Barrett, T., Troup, D. B., Wilhite, S. E., Ledoux, P., Evangelista, C., Kim, I. F., Tomashevsky, M., Marshall, K. A., Phillippy, K. H., Sherman, P. M., Muertter, R. N., Holko, M., Ayanbule, O., Yefanov, A., and Soboleva, A. (2011). NCBI GEO: archive for functional genomics data sets – 10 years on. Nucleic Acids Res. 39, D1005–D1010.| NCBI GEO: archive for functional genomics data sets – 10 years on.Crossref | GoogleScholarGoogle Scholar | 21097893PubMed |
Belarbi, Y., Mejhert, N., Gao, H., Arner, P., Ryden, M., and Kulyte, A. (2018). MicroRNAs-361-5p and miR-574-5p associate with human adipose morphology and regulate EBF1 expression in white adipose tissue. Mol. Cell. Endocrinol. 472, 50–56.
| MicroRNAs-361-5p and miR-574-5p associate with human adipose morphology and regulate EBF1 expression in white adipose tissue.Crossref | GoogleScholarGoogle Scholar | 29191698PubMed |
Chang, C. W., Yu, J. C., Hsieh, Y. H., Yao, C. C., Chao, J. I., Chen, P. M., Hsieh, H. Y., Hsiung, C. N., Chu, H. W., Shen, C. Y., and Cheng, C. W. (2016a). MicroRNA-30a increases tight junction protein expression to suppress the epithelial–mesenchymal transition and metastasis by targeting Slug in breast cancer. Oncotarget 7, 16462–16478.
| MicroRNA-30a increases tight junction protein expression to suppress the epithelial–mesenchymal transition and metastasis by targeting Slug in breast cancer.Crossref | GoogleScholarGoogle Scholar | 26918943PubMed |
Chang, T., Xie, J., Li, H., Li, D., Liu, P., and Hu, Y. (2016b). MicroRNA-30a promotes extracellular matrix degradation in articular cartilage via downregulation of Sox9. Cell Prolif. 49, 207–218.
| MicroRNA-30a promotes extracellular matrix degradation in articular cartilage via downregulation of Sox9.Crossref | GoogleScholarGoogle Scholar | 26969024PubMed |
Chen, X., Gao, C., Li, H., Huang, L., Sun, Q., Dong, Y., Tian, C., Gao, S., Dong, H., Guan, D., Hu, X., Zhao, S., Li, L., Zhu, L., Yan, Q., Zhang, J., Zen, K., and Zhang, C. Y. (2010). Identification and characterization of microRNAs in raw milk during different periods of lactation, commercial fluid, and powdered milk products. Cell Res. 20, 1128–1137.
| Identification and characterization of microRNAs in raw milk during different periods of lactation, commercial fluid, and powdered milk products.Crossref | GoogleScholarGoogle Scholar | 20548333PubMed |
Chen, Y., Wang, J., Yang, S., Utturkar, S., Crodian, J., Cummings, S., Thimmapuram, J., San Miguel, P., Kuang, S., Gribskov, M., Plaut, K., and Casey, T. (2017a). Effect of high-fat diet on secreted milk transcriptome in midlactation mice. Physiol. Genomics 49, 747–762.
| Effect of high-fat diet on secreted milk transcriptome in midlactation mice.Crossref | GoogleScholarGoogle Scholar | 29093195PubMed |
Chen, Z., Luo, J., Sun, S., Cao, D., Shi, H., and Loor, J. J. (2017b). miR-148a and miR-17-5p synergistically regulate milk TAG synthesis via PPARGC1A and PPARA in goat mammary epithelial cells. RNA Biol. 14, 326–338.
| miR-148a and miR-17-5p synergistically regulate milk TAG synthesis via PPARGC1A and PPARA in goat mammary epithelial cells.Crossref | GoogleScholarGoogle Scholar | 28095188PubMed |
Cheng, C. W., Wang, H. W., Chang, C. W., Chu, H. W., Chen, C. Y., Yu, J. C., Chao, J. I., Liu, H. F., Ding, S. L., and Shen, C. Y. (2012). MicroRNA-30a inhibits cell migration and invasion by downregulating vimentin expression and is a potential prognostic marker in breast cancer. Breast Cancer Res. Treat. 134, 1081–1093.
| MicroRNA-30a inhibits cell migration and invasion by downregulating vimentin expression and is a potential prognostic marker in breast cancer.Crossref | GoogleScholarGoogle Scholar | 22476851PubMed |
Eguchi, T., Watanabe, K., Hara, E. S., Ono, M., Kuboki, T., and Calderwood, S. K. (2013). OstemiR: a novel panel of microRNA biomarkers in osteoblastic and osteocytic differentiation from mesencymal stem cells. PLoS One 8, e58796.
| OstemiR: a novel panel of microRNA biomarkers in osteoblastic and osteocytic differentiation from mesencymal stem cells.Crossref | GoogleScholarGoogle Scholar | 24386225PubMed |
Elyakim, E., Sitbon, E., Faerman, A., Tabak, S., Montia, E., Belanis, L., Dov, A., Marcusson, E. G., Bennett, C. F., Chajut, A., Cohen, D., and Yerushalmi, N. (2010). hsa-miR-191 is a candidate oncogene target for hepatocellular carcinoma therapy. Cancer Res. 70, 8077–8087.
| hsa-miR-191 is a candidate oncogene target for hepatocellular carcinoma therapy.Crossref | GoogleScholarGoogle Scholar | 20924108PubMed |
ElShamy, W. M. (2016). The protective effect of longer duration of breastfeeding against pregnancy-associated triple negative breast cancer. Oncotarget 7, 53941–53950.
| The protective effect of longer duration of breastfeeding against pregnancy-associated triple negative breast cancer.Crossref | GoogleScholarGoogle Scholar | 27248476PubMed |
Faupel-Badger, J. M., Arcaro, K. F., Balkam, J. J., Eliassen, A. H., Hassiotou, F., Lebrilla, C. B., Michels, K. B., Palmer, J. R., Schedin, P., Stuebe, A. M., Watson, C. J., and Sherman, M. E. (2013). Postpartum remodeling, lactation, and breast cancer risk: summary of a National Cancer Institute-sponsored workshop. J. Natl Cancer Inst. 105, 166–174.
| Postpartum remodeling, lactation, and breast cancer risk: summary of a National Cancer Institute-sponsored workshop.Crossref | GoogleScholarGoogle Scholar | 23264680PubMed |
Fu, J., Xu, X., Kang, L., Zhou, L., Wang, S., Lu, J., Cheng, L., Fan, Z., Yuan, B., Tian, P., Zheng, X., Yu, C., Ye, Q., and Lv, Z. (2014). miR-30a suppresses breast cancer cell proliferation and migration by targeting Eya2. Biochem. Biophys. Res. Commun. 445, 314–319.
| miR-30a suppresses breast cancer cell proliferation and migration by targeting Eya2.Crossref | GoogleScholarGoogle Scholar | 24508260PubMed |
Gailhouste, L., Gomez-Santos, L., Hagiwara, K., Hatada, I., Kitagawa, N., Kawaharada, K., Thirion, M., Kosaka, N., Takahashi, R. U., Shibata, T., Miyajima, A., and Ochiya, T. (2013). miR-148a plays a pivotal role in the liver by promoting the hepatospecific phenotype and suppressing the invasiveness of transformed cells. Hepatology 58, 1153–1165.
| miR-148a plays a pivotal role in the liver by promoting the hepatospecific phenotype and suppressing the invasiveness of transformed cells.Crossref | GoogleScholarGoogle Scholar | 23532995PubMed |
Gilam, A., Shai, A., Ashkenazi, I., Sarid, L. A., Drobot, A., Bickel, A., and Shomron, N. (2017). MicroRNA regulation of progesterone receptor in breast cancer. Oncotarget 8, 25963–25976.
| MicroRNA regulation of progesterone receptor in breast cancer.Crossref | GoogleScholarGoogle Scholar | 28404930PubMed |
Goedeke, L., Rotllan, N., Canfran-Duque, A., Aranda, J. F., Ramirez, C. M., Araldi, E., Lin, C. S., Anderson, N. N., Wagschal, A., de Cabo, R., Horton, J. D., Lasuncion, M. A., Naar, A. M., Suarez, Y., and Fernandez-Hernando, C. (2015). MicroRNA-148a regulates LDL receptor and ABCA1 expression to control circulating lipoprotein levels. Nat. Med. 21, 1280–1289.
| MicroRNA-148a regulates LDL receptor and ABCA1 expression to control circulating lipoprotein levels.Crossref | GoogleScholarGoogle Scholar | 26437365PubMed |
Gu, Y., Li, M., Wang, T., Liang, Y., Zhong, Z., Wang, X., Zhou, Q., Chen, L., Lang, Q., He, Z., Chen, X., Gong, J., Gao, X., Li, X., and Lv, X. (2012). Lactation-related microRNA expression profiles of porcine breast milk exosomes. PLoS One 7, e43691.
| Lactation-related microRNA expression profiles of porcine breast milk exosomes.Crossref | GoogleScholarGoogle Scholar | 23300774PubMed |
Hata, T., Murakami, K., Nakatani, H., Yamamoto, Y., Matsuda, T., and Aoki, N. (2010). Isolation of bovine milk-derived microvesicles carrying mRNAs and microRNAs. Biochem. Biophys. Res. Commun. 396, 528–533.
| Isolation of bovine milk-derived microvesicles carrying mRNAs and microRNAs.Crossref | GoogleScholarGoogle Scholar | 20434431PubMed |
Hackenberg, M., Sturm, M., Langenberger, D., Falcón-Pérez, J. M., and Aransay, A. M. (2009). miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments. Nucleic Acids Res. 37, W68–W76.
| miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments.Crossref | GoogleScholarGoogle Scholar | 19433510PubMed |
Hackenberg, M., Rodríguez-Ezpeleta, N., and Aransay, A. M. (2011). miRanalyzer: an update on the detection and analysis of microRNAs in high-throughput sequencing experiments. Nucleic Acids Res. 39, W132–W138.
| miRanalyzer: an update on the detection and analysis of microRNAs in high-throughput sequencing experiments.Crossref | GoogleScholarGoogle Scholar | 21515631PubMed |
Huang, F., Zhao, J. L., Wang, L., Gao, C. C., Liang, S. Q., An, D. J., Bai, J., Chen, Y., Han, H., and Qin, H. Y. (2017). miR-148a-3p mediates notch signaling to promote the differentiation and M1 activation of macrophages. Front. Immunol. 8, 1327.
| miR-148a-3p mediates notch signaling to promote the differentiation and M1 activation of macrophages.Crossref | GoogleScholarGoogle Scholar | 29085372PubMed |
Islami, F., Liu, Y., Jemal, A., Zhou, J., Weiderpass, E., Colditz, G., Boffetta, P., and Weiss, M. (2015). Breastfeeding and breast cancer risk by receptor status – a systematic review and meta-analysis. Ann. Oncol. 26, 2398–2407.
| 26504151PubMed |
Jiang, Q., Lagos-Quintana, M., Liu, D., Shi, Y., Helker, C., Herzog, W., and le Noble, F. (2013). miR-30a regulates endothelial tip cell formation and arteriolar branching. Hypertension 62, 592–598.
| miR-30a regulates endothelial tip cell formation and arteriolar branching.Crossref | GoogleScholarGoogle Scholar | 23817492PubMed |
Joshi, P., Jeon, Y. J., Lagana, A., Middleton, J., Secchiero, P., Garofalo, M., and Croce, C. M. (2015). MicroRNA-148a reduces tumorigenesis and increases TRAIL-induced apoptosis in NSCLC. Proc. Natl Acad. Sci. USA 112, 8650–8655.
| MicroRNA-148a reduces tumorigenesis and increases TRAIL-induced apoptosis in NSCLC.Crossref | GoogleScholarGoogle Scholar | 26124099PubMed |
Koh, E. H., Chen, Y., Bader, D. A., Hamilton, M. P., He, B., York, B., Kajimura, S., McGuire, S. E., and Hartig, S. M. (2016). Mitochondrial activity in human white adipocytes is regulated by the ubiquitin carrier protein 9/microRNA-30a axis. J. Biol. Chem. 291, 24747–24755.
| Mitochondrial activity in human white adipocytes is regulated by the ubiquitin carrier protein 9/microRNA-30a axis.Crossref | GoogleScholarGoogle Scholar | 27758866PubMed |
Kosaka, N., Izumi, H., Sekine, K., and Ochiya, T. (2010). MicroRNA as a new immune-regulatory agent in breast milk. Silence 1, 7.
| MicroRNA as a new immune-regulatory agent in breast milk.Crossref | GoogleScholarGoogle Scholar | 20226005PubMed |
Kurozumi, S., Yamaguchi, Y., Kurosumi, M., Ohira, M., Matsumoto, H., and Horiguchi, J. (2017). Recent trends in microRNA research into breast cancer with particular focus on the associations between microRNAs and intrinsic subtypes. J. Hum. Genet. 62, 15–24.
| Recent trends in microRNA research into breast cancer with particular focus on the associations between microRNAs and intrinsic subtypes.Crossref | GoogleScholarGoogle Scholar | 27439682PubMed |
Lee, H., Han, S., Kwon, C. S., and Lee, D. (2016). Biogenesis and regulation of the let-7 miRNAs and their functional implications. Protein Cell 7, 100–113.
| Biogenesis and regulation of the let-7 miRNAs and their functional implications.Crossref | GoogleScholarGoogle Scholar | 26399619PubMed |
Li, X., Liu, L., Yang, J., Yu, Y., Chai, J., Wang, L., Ma, L., and Yin, H. (2016a). Exosome derived from human umbilical cord mesenchymal stem cell mediates miR-181c attenuating burn-induced excessive inflammation. EBioMedicine 8, 72–82.
| Exosome derived from human umbilical cord mesenchymal stem cell mediates miR-181c attenuating burn-induced excessive inflammation.Crossref | GoogleScholarGoogle Scholar | 27428420PubMed |
Li, Y., Deng, X., Zeng, X., and Peng, X. (2016b). The role of miR-148a in cancer. J. Cancer 7, 1233–1241.
| The role of miR-148a in cancer.Crossref | GoogleScholarGoogle Scholar | 27390598PubMed |
Li, Q., Ren, P., Shi, P., Chen, Y., Xiang, F., Zhang, L., Wang, J., Lv, Q., and Xie, M. (2017). MicroRNA-148a promotes apoptosis and suppresses growth of breast cancer cells by targeting B-cell lymphoma 2. Anticancer Drugs 28, 588–595.
| MicroRNA-148a promotes apoptosis and suppresses growth of breast cancer cells by targeting B-cell lymphoma 2.Crossref | GoogleScholarGoogle Scholar | 28430743PubMed |
Long, G., Wang, F., Duan, Q., Yang, S., Chen, F., Gong, W., Yang, X., Wang, Y., Chen, C., and Wang, D. W. (2012). Circulating miR-30a, miR-195 and let-7b associated with acute myocardial infarction. PLoS One 7, e50926.
| Circulating miR-30a, miR-195 and let-7b associated with acute myocardial infarction.Crossref | GoogleScholarGoogle Scholar | 23236408PubMed |
McCarthy, D. J., Chen, Y., and Smyth, G. K. (2012). Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 40, 4288–4297.
| Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation.Crossref | GoogleScholarGoogle Scholar | 22287627PubMed |
Modepalli, V., Kumar, A., Hinds, L. A., Sharp, J. A., Nicholas, K. R., and Lefevre, C. (2014). Differential temporal expression of milk miRNA during the lactation cycle of the marsupial tammar wallaby (Macropus eugenii). BMC Genomics 15, 1012.
| Differential temporal expression of milk miRNA during the lactation cycle of the marsupial tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 25417092PubMed |
Muroya, S., Hagi, T., Kimura, A., Aso, H., Matsuzaki, M., and Nomura, M. (2016). Lactogenic hormones alter cellular and extracellular microRNA expression in bovine mammary epithelial cell culture. J. Anim. Sci. Biotechnol. 7, 8.
| Lactogenic hormones alter cellular and extracellular microRNA expression in bovine mammary epithelial cell culture.Crossref | GoogleScholarGoogle Scholar | 26889380PubMed |
O’Brien, J. H., Hernandez-Lagunas, L., Artinger, K. B., and Ford, H. L. (2014). MicroRNA-30a regulates zebrafish myogenesis through targeting the transcription factor Six1. J. Cell Sci. 127, 2291–2301.
| MicroRNA-30a regulates zebrafish myogenesis through targeting the transcription factor Six1.Crossref | GoogleScholarGoogle Scholar | 24634509PubMed |
Ouzounova, M., Vuong, T., Ancey, P. B., Ferrand, M., Durand, G., Le-Calvez Kelm, F., Croce, C., Matar, C., Herceg, Z., and Hernandez-Vargas, H. (2013). MicroRNA miR-30 family regulates non-attachment growth of breast cancer cells. BMC Genomics 14, 139.
| MicroRNA miR-30 family regulates non-attachment growth of breast cancer cells.Crossref | GoogleScholarGoogle Scholar | 23445407PubMed |
Pan, W., Zhong, Y., Cheng, C., Liu, B., Wang, L., Li, A., Xiong, L., and Liu, S. (2013). MiR-30-regulated autophagy mediates angiotensin II-induced myocardial hypertrophy. PLoS One 8, e53950.
| MiR-30-regulated autophagy mediates angiotensin II-induced myocardial hypertrophy.Crossref | GoogleScholarGoogle Scholar | 24312475PubMed |
Peng, R., Zhou, L., Zhou, Y., Zhao, Y., Li, Q., Ni, D., Hu, Y., Long, Y., Liu, J., Lyu, Z., Mao, Z., Yuan, Y., Huang, L., Zhao, H., Li, G., and Zhou, Q. (2015). MiR-30a inhibits the epithelial–mesenchymal transition of podocytes through downregulation of NFATc3. Int. J. Mol. Sci. 16, 24032–24047.
| MiR-30a inhibits the epithelial–mesenchymal transition of podocytes through downregulation of NFATc3.Crossref | GoogleScholarGoogle Scholar | 26473838PubMed |
Perri, M., Lucente, M., Cannataro, R., De Luca, I. F., Gallelli, L., Moro, G., De Sarro, G., Caroleo, M. C., and Cione, E. (2018). Variation in immune-related microRNAs profile in human milk amongst lactating women. MicroRNA 7, 107–114.
| Variation in immune-related microRNAs profile in human milk amongst lactating women.Crossref | GoogleScholarGoogle Scholar | 29412128PubMed |
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., and Smyth, G. K. (2015). limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47.
| limma powers differential expression analyses for RNA-sequencing and microarray studies.Crossref | GoogleScholarGoogle Scholar | 25925576PubMed |
Robinson, M. D., McCarthy, D. J., and Smyth, G. K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140.
| edgeR: a Bioconductor package for differential expression analysis of digital gene expression data.Crossref | GoogleScholarGoogle Scholar | 19910308PubMed |
Sharp, J. A., Mailer, S. L., Thomson, P. C., Lefèvre, C., and Nicholas, K. R. (2008). Identification and transcript analysis of a novel wallaby (Macropus eugenii) basal-like breast cancer cell line. Mol. Cancer 7, 1–15.
| Identification and transcript analysis of a novel wallaby (Macropus eugenii) basal-like breast cancer cell line.Crossref | GoogleScholarGoogle Scholar | 18179684PubMed |
Shen, J., DiCioccio, R., Odunsi, K., Lele, S. B., and Zhao, H. (2010). Novel genetic variants in miR-191 gene and familial ovarian cancer. BMC Cancer 10, 47–55.
| Novel genetic variants in miR-191 gene and familial ovarian cancer.Crossref | GoogleScholarGoogle Scholar | 20167074PubMed |
Shi, C., Zhang, M., Tong, M., Yang, L., Pang, L., Chen, L., Xu, G., Chi, X., Hong, Q., Ni, Y., Ji, C., and Guo, X. (2015). miR-148a is associated with obesity and modulates adipocyte differentiation of mesenchymal stem cells through Wnt signaling. Sci. Rep. 5, 9930.
| miR-148a is associated with obesity and modulates adipocyte differentiation of mesenchymal stem cells through Wnt signaling.Crossref | GoogleScholarGoogle Scholar | 26001136PubMed |
Sun, J., Aswath, K., Schroeder, S. G., Lippolis, J. D., Reinhardt, T. A., and Sonstegard, T. S. (2015). MicroRNA expression profiles of bovine milk exosomes in response to Staphylococcus aureus infection. BMC Genomics 16, 806.
| MicroRNA expression profiles of bovine milk exosomes in response to Staphylococcus aureus infection.Crossref | GoogleScholarGoogle Scholar | 26475455PubMed |
Tian, Y., Guo, R., Shi, B., Chen, L., Yang, L., and Fu, Q. (2016). MicroRNA-30a promotes chondrogenic differentiation of mesenchymal stem cells through inhibiting Delta-like 4 expression. Life Sci. 148, 220–228.
| MicroRNA-30a promotes chondrogenic differentiation of mesenchymal stem cells through inhibiting Delta-like 4 expression.Crossref | GoogleScholarGoogle Scholar | 26872979PubMed |
Vonk, L. A., Kragten, A. H., Dhert, W. J., Saris, D. B., and Creemers, L. B. (2014). Overexpression of hsa-miR-148a promotes cartilage production and inhibits cartilage degradation by osteoarthritic chondrocytes. Osteoarthritis Cartilage 22, 145–153.
| Overexpression of hsa-miR-148a promotes cartilage production and inhibits cartilage degradation by osteoarthritic chondrocytes.Crossref | GoogleScholarGoogle Scholar | 24269634PubMed |
Wang, B., Komers, R., Carew, R., Winbanks, C. E., Xu, B., Herman-Edelstein, M., Koh, P., Thomas, M., Jandeleit-Dahm, K., Gregorevic, P., Cooper, M. E., and Kantharidis, P. (2012). Suppression of microRNA-29 expression by TGF-beta1 promotes collagen expression and renal fibrosis. J. Am. Soc. Nephrol. 23, 252–265.
| Suppression of microRNA-29 expression by TGF-beta1 promotes collagen expression and renal fibrosis.Crossref | GoogleScholarGoogle Scholar | 22095944PubMed |
Wang, Z., Dai, X., Chen, Y., Sun, C., Zhu, Q., Zhao, H., Liu, G., Huang, Q., and Lan, Q. (2015). MiR-30a-5p is induced by Wnt/beta-catenin pathway and promotes glioma cell invasion by repressing NCAM. Biochem. Biophys. Res. Commun. 465, 374–380.
| MiR-30a-5p is induced by Wnt/beta-catenin pathway and promotes glioma cell invasion by repressing NCAM.Crossref | GoogleScholarGoogle Scholar | 26255203PubMed |
Wang, X., Liang, Z., Xu, X., Li, J., Zhu, Y., Meng, S., Li, S., Wang, S., Xie, B., Ji, A., Liu, B., Zheng, X., and Xie, L. (2016). miR-148a-3p represses proliferation and EMT by establishing regulatory circuits between ERBB3/AKT2/c-myc and DNMT1 in bladder cancer. Cell Death Dis. 7, e2503.
| miR-148a-3p represses proliferation and EMT by establishing regulatory circuits between ERBB3/AKT2/c-myc and DNMT1 in bladder cancer.Crossref | GoogleScholarGoogle Scholar | 27929537PubMed |
Weber, J. A., Baxter, D. H., Zhang, S., Huang, D. Y., Huang, K. H., Lee, M. J., Galas, D. J., and Wang, K. (2010). The microRNA spectrum in 12 body fluids. Clin. Chem. 56, 1733–1741.
| The microRNA spectrum in 12 body fluids.Crossref | GoogleScholarGoogle Scholar | 20847327PubMed |
Weitzel, R. P., Lesniewski, M. L., Haviernik, P., Kadereit, S., Leahy, P., Greco, N. J., and Laughlin, M. J. (2009). microRNA 184 regulates expression of NFAT1 in umbilical cord blood CD4+ T cells. Blood 113, 6648–6657.
| microRNA 184 regulates expression of NFAT1 in umbilical cord blood CD4+ T cells.Crossref | GoogleScholarGoogle Scholar | 19286996PubMed |
Winsel, S., Maki-Jouppila, J., Tambe, M., Aure, M. R., Pruikkonen, S., Salmela, A. L., Halonen, T., Leivonen, S. K., Kallio, L., Borresen-Dale, A. L., and Kallio, M. J. (2014). Excess of miRNA-378a-5p perturbs mitotic fidelity and correlates with breast cancer tumourigenesis in vivo. Br. J. Cancer 111, 2142–2151.
| Excess of miRNA-378a-5p perturbs mitotic fidelity and correlates with breast cancer tumourigenesis in vivo.Crossref | GoogleScholarGoogle Scholar | 25268374PubMed |
Wu, Z., Huang, X., Huang, X., Zou, Q., and Guo, Y. (2013). The inhibitory role of miR-29 in growth of breast cancer cells. J. Exp. Clin. Cancer Res. 32, 98.
| The inhibitory role of miR-29 in growth of breast cancer cells.Crossref | GoogleScholarGoogle Scholar | 24289849PubMed |
Xie, H., Lin, H. L., Wang, N., Sun, Y. L., Kan, Y., Guo, H., Chen, J. L., and Fang, M. (2015). Inhibition of microRNA-30a prevents puromycin aminonucleoside-induced podocytic apoptosis by upregulating the glucocorticoid receptor alpha. Mol. Med. Rep. 12, 6043–6052.
| Inhibition of microRNA-30a prevents puromycin aminonucleoside-induced podocytic apoptosis by upregulating the glucocorticoid receptor alpha.Crossref | GoogleScholarGoogle Scholar | 26299668PubMed |
Xu, X., Zhang, Y., Jasper, J., Lykken, E., Alexander, P. B., Markowitz, G. J., McDonnell, D. P., Li, Q. J., and Wang, X. F. (2016). MiR-148a functions to suppress metastasis and serves as a prognostic indicator in triple-negative breast cancer. Oncotarget 7, 20381–20394.
| MiR-148a functions to suppress metastasis and serves as a prognostic indicator in triple-negative breast cancer.Crossref | GoogleScholarGoogle Scholar | 26967387PubMed |
Yang, X., Chen, Y., and Chen, L. (2017a). The versatile role of microRNA-30a in human cancer. Cell. Physiol. Biochem. 41, 1616–1632.
| The versatile role of microRNA-30a in human cancer.Crossref | GoogleScholarGoogle Scholar | 28359057PubMed |
Yang, C., Tabatabaei, S. N., Ruan, X., and Hardy, P. (2017b). The dual regulatory role of MiR-181a in breast cancer. Cell. Physiol. Biochem. 44, 843–856.
| The dual regulatory role of MiR-181a in breast cancer.Crossref | GoogleScholarGoogle Scholar | 29176320PubMed |
Zhang, J., Ying, Z. Z., Tang, Z. L., Long, L. Q., and Li, K. (2012). MicroRNA-148a promotes myogenic differentiation by targeting the ROCK1 gene. J. Biol. Chem. 287, 21093–21101.
| MicroRNA-148a promotes myogenic differentiation by targeting the ROCK1 gene.Crossref | GoogleScholarGoogle Scholar | 22547064PubMed |
Zhang, R., Weng, Y., Li, B., Jiang, Y., Yan, S., He, F., Chen, X., Deng, F., Wang, J., and Shi, Q. (2015). BMP9-induced osteogenic differentiation is partially inhibited by miR-30a in the mesenchymal stem cell line C3H10T1/2. J. Mol. Histol. 46, 399–407.
| BMP9-induced osteogenic differentiation is partially inhibited by miR-30a in the mesenchymal stem cell line C3H10T1/2.Crossref | GoogleScholarGoogle Scholar | 26205653PubMed |
Zhou, Q., Li, M., Wang, X., Li, Q., Wang, T., Zhu, Q., Zhou, X., Gao, X., and Li, X. (2012). Immune-related microRNAs are abundant in breast milk exosomes. Int. J. Biol. Sci. 8, 118–123.
| Immune-related microRNAs are abundant in breast milk exosomes.Crossref | GoogleScholarGoogle Scholar | 22211110PubMed |
