{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T15:11:51Z","timestamp":1785856311881,"version":"3.56.0"},"reference-count":130,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2021,2,26]],"date-time":"2021-02-26T00:00:00Z","timestamp":1614297600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100005010","name":"Associazione Italiana per la Ricerca sul Cancro","doi-asserted-by":"publisher","award":["20505"],"award-info":[{"award-number":["20505"]}],"id":[{"id":"10.13039\/501100005010","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Teneurins have been identified in vertebrates as four different genes (TENM1-4), coding for membrane proteins that are mainly involved in embryonic and neuronal development. Genetic studies have correlated them with various diseases, including developmental problems, neurological disorders and congenital general anosmia. There is some evidence to suggest their possible involvement in cancer initiation and progression, and drug resistance. Indeed, mutations, chromosomal alterations and the deregulation of teneurins expression have been associated with several tumor types and patient survival. However, the role of teneurins in cancer-related regulatory networks is not fully understood, as both a tumor-suppressor role and pro-tumoral functions have been proposed, depending on tumor histotype. Here, we summarize and discuss the literature data on teneurins expression and their potential role in different tumor types, while highlighting the possibility of using teneurins as novel molecular diagnostic and prognostic biomarkers and as targets for cancer treatments, such as immunotherapy, in some tumors.<\/jats:p>","DOI":"10.3390\/ijms22052321","type":"journal-article","created":{"date-parts":[[2021,2,26]],"date-time":"2021-02-26T04:36:24Z","timestamp":1614314184000},"page":"2321","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":41,"title":["Teneurins: Role in Cancer and Potential Role as Diagnostic Biomarkers and Targets for Therapy"],"prefix":"10.3390","volume":"22","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1103-6079","authenticated-orcid":false,"given":"Giulia","family":"Peppino","sequence":"first","affiliation":[{"name":"Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Via Nizza 52, 10126 Torino, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0431-2656","authenticated-orcid":false,"given":"Roberto","family":"Ruiu","sequence":"additional","affiliation":[{"name":"Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Via Nizza 52, 10126 Torino, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maddalena","family":"Arigoni","sequence":"additional","affiliation":[{"name":"Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Via Nizza 52, 10126 Torino, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9692-0172","authenticated-orcid":false,"given":"Federica","family":"Riccardo","sequence":"additional","affiliation":[{"name":"Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Via Nizza 52, 10126 Torino, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonella","family":"Iacoviello","sequence":"additional","affiliation":[{"name":"Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Via Nizza 52, 10126 Torino, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5698-0202","authenticated-orcid":false,"given":"Giuseppina","family":"Barutello","sequence":"additional","affiliation":[{"name":"Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Via Nizza 52, 10126 Torino, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8151-9124","authenticated-orcid":false,"given":"Elena","family":"Quaglino","sequence":"additional","affiliation":[{"name":"Molecular Biotechnology Center, Department of Molecular Biotechnology and Health Sciences, University of Torino, Via Nizza 52, 10126 Torino, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,2,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"990","DOI":"10.1016\/j.biocel.2008.06.014","article-title":"Teneurins: Important regulators of neural circuitry","volume":"41","author":"Young","year":"2009","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1006\/dbio.1999.9503","article-title":"Teneurins: A novel family of neuronal cell surface proteins in vertebrates, homologous to the Drosophila pair-rule gene product Ten-m","volume":"216","author":"Rubin","year":"1999","journal-title":"Dev. Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2957","DOI":"10.1242\/jcs.00603","article-title":"The intracellular domain of teneurin-2 has a nuclear function and represses zic-1-mediated transcription","volume":"116 Pt 14","author":"Bagutti","year":"2003","journal-title":"J. Cell Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1016\/j.yexcr.2004.12.020","article-title":"The intracellular domain of teneurin-1 interacts with MBD1 and CAP\/ponsin resulting in subcellular codistribution and translocation to the nuclear matrix","volume":"305","author":"Nunes","year":"2005","journal-title":"Exp. Cell Res."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Kenzelmann, D., Chiquet-Ehrismann, R., Leachman, N.T., and Tucker, R.P. (2008). Teneurin-1 is expressed in interconnected regions of the developing brain and is processed in vivo. BMC Dev. Biol., 8.","DOI":"10.1186\/1471-213X-8-30"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3619","DOI":"10.1093\/emboj\/17.13.3619","article-title":"Identification of novel stress-induced genes downstream of chop","volume":"17","author":"Wang","year":"1998","journal-title":"EMBO J."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"3728","DOI":"10.1002\/j.1460-2075.1994.tb06682.x","article-title":"Tenm, a Drosophila gene related to tenascin, is a new pair-rule gene","volume":"13","author":"Baumgartner","year":"1994","journal-title":"EMBO J."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1016\/0092-8674(94)90220-8","article-title":"Odd Oz: A novel Drosophila pair rule gene","volume":"77","author":"Levine","year":"1994","journal-title":"Cell"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Zheng, L., Michelson, Y., Freger, V., Avraham, Z., Venken, K.J., Bellen, H.J., Justice, M.J., and Wides, R. (2011). Drosophila Ten-m and filamin affect motor neuron growth cone guidance. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0022956"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/S0925-4773(02)00055-2","article-title":"Expression of Drosophila Ten-a, a dimeric receptor during embryonic development","volume":"114","author":"Fascetti","year":"2002","journal-title":"Mech. Dev."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1186\/s41065-017-0029-1","article-title":"Ancient role of ten-m\/odz in segmentation and the transition from sequential to syncytial segmentation","volume":"154","author":"Hunding","year":"2017","journal-title":"Hereditas"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1006\/dbio.1999.9532","article-title":"The mammalian Odz gene family: Homologs of a Drosophila pair-rule gene with expression implying distinct yet overlapping developmental roles","volume":"217","author":"Feige","year":"2000","journal-title":"Dev. Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/j.mcn.2006.06.012","article-title":"Potential target genes of EMX2 include Odz\/Ten-M and other gene families with implications for cortical patterning","volume":"33","author":"Li","year":"2006","journal-title":"Mol. Cell Neurosci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1016\/S1567-133X(03)00087-5","article-title":"The murine Ten-m\/Odz genes show distinct but overlapping expression patterns during development and in adult brain","volume":"3","author":"Zhou","year":"2003","journal-title":"Gene Expr. Patterns"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1111\/ejn.12767","article-title":"The glycoprotein Ten-m3 mediates topography and patterning of thalamostriatal projections from the parafascicular nucleus in mice","volume":"41","author":"Tran","year":"2015","journal-title":"Eur. J. Neurosci."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Bibollet-Bahena, O., Okafuji, T., Hokamp, K., Tear, G., and Mitchell, K.J. (2017). A dual-strategy expression screen for candidate connectivity labels in the developing thalamus. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0177977"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"146","DOI":"10.3389\/fnins.2015.00146","article-title":"Ancient interaction between the teneurin C-terminal associated peptides (TCAP) and latrophilin ligand-receptor coupling: A role in behavior","volume":"9","author":"Woelfle","year":"2015","journal-title":"Front. Neurosci."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Ferralli, J., Tucker, R.P., and Chiquet-Ehrismann, R. (2018). The teneurin C-terminal domain possesses nuclease activity and is apoptogenic. Biol. Open, 7.","DOI":"10.1242\/bio.031765"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"938","DOI":"10.3389\/fnins.2018.00938","article-title":"Teneurins: Domain Architecture, Evolutionary Origins, and Patterns of Expression","volume":"12","author":"Tucker","year":"2018","journal-title":"Front. Neurosci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1083\/jcb.145.3.563","article-title":"Mouse ten-m\/Odz is a new family of dimeric type II transmembrane proteins expressed in many tissues","volume":"145","author":"Oohashi","year":"1999","journal-title":"J. Cell Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.sbi.2019.01.028","article-title":"Teneurins and latrophilins: Two giants meet at the synapse","volume":"54","author":"Arac","year":"2019","journal-title":"Curr. Opin. Struct. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1038\/nature10926","article-title":"Teneurins instruct synaptic partner matching in an olfactory map","volume":"484","author":"Hong","year":"2012","journal-title":"Nature"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1038\/nature10923","article-title":"Trans-synaptic Teneurin signalling in neuromuscular synapse organization and target choice","volume":"484","author":"Mosca","year":"2012","journal-title":"Nature"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"204","DOI":"10.3389\/fncel.2015.00204","article-title":"On the Teneurin track: A new synaptic organization molecule emerges","volume":"9","author":"Mosca","year":"2015","journal-title":"Front. Cell Neurosci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1452","DOI":"10.1007\/s00018-007-7108-9","article-title":"Teneurins, a transmembrane protein family involved in cell communication during neuronal development","volume":"64","author":"Kenzelmann","year":"2007","journal-title":"Cell Mol. Life Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"26128","DOI":"10.1074\/jbc.M203722200","article-title":"All four members of the Ten-m\/Odz family of transmembrane proteins form dimers","volume":"277","author":"Feng","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"12113","DOI":"10.1073\/pnas.1019434108","article-title":"Latrophilin 1 and its endogenous ligand Lasso\/teneurin-2 form a high-affinity transsynaptic receptor pair with signaling capabilities","volume":"108","author":"Silva","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1074\/jbc.M113.504779","article-title":"Latrophilins function as heterophilic cell-adhesion molecules by binding to teneurins: Regulation by alternative splicing","volume":"289","author":"Boucard","year":"2014","journal-title":"J. Biol. Chem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1016\/j.cell.2018.03.036","article-title":"Structural Basis for Teneurin Function in Circuit-Wiring: A Toxin Motif at the Synapse","volume":"173","author":"Li","year":"2018","journal-title":"Cell"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/j.cell.2019.12.014","article-title":"Structural Basis of Teneurin-Latrophilin Interaction in Repulsive Guidance of Migrating Neurons","volume":"180","author":"Chu","year":"2020","journal-title":"Cell"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1038\/nature25463","article-title":"Teneurin-3 controls topographic circuit assembly in the hippocampus","volume":"554","author":"Berns","year":"2018","journal-title":"Nature"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1002\/1097-0177(2000)9999:9999<::AID-DVDY1084>3.0.CO;2-B","article-title":"Teneurin-2 is expressed in tissues that regulate limb and somite pattern formation and is induced in vitro and in situ by FGF8","volume":"220","author":"Tucker","year":"2001","journal-title":"Dev. Dyn."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/j.ygcen.2004.02.007","article-title":"Cloning and characterization of teneurin C-terminus associated peptide (TCAP)-3 from the hypothalamus of an adult rainbow trout (Oncorhynchus mykiss)","volume":"137","author":"Qian","year":"2004","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.canlet.2012.07.021","article-title":"Teneurin protein family: An emerging role in human tumorigenesis and drug resistance","volume":"326","author":"Ziegler","year":"2012","journal-title":"Cancer Lett."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"937","DOI":"10.3389\/fnins.2018.00937","article-title":"Teneurins: An Integrative Molecular, Functional, and Biomedical Overview of Their Role in Cancer","volume":"12","author":"Ziegler","year":"2018","journal-title":"Front. Neurosci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1111\/cge.12782","article-title":"A role for TENM1 mutations in congenital general anosmia","volume":"90","author":"Alkelai","year":"2016","journal-title":"Clin. Genet."},{"key":"ref_37","first-page":"1356","article-title":"A novel adaptor protein family regulating cytoskeletal organization and signal transduction\u2014Vinexin, CAP\/ponsin, ArgBP2","volume":"74","author":"Kioka","year":"2002","journal-title":"Seikagaku"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"581","DOI":"10.3389\/fnins.2019.00581","article-title":"Activity of the Carboxy-Terminal Peptide Region of the Teneurins and Its Role in Neuronal Function and Behavior in Mammals","volume":"13","author":"Hogg","year":"2019","journal-title":"Front. Neurosci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.brainres.2007.07.087","article-title":"Teneurin carboxy (C)-terminal associated peptide-1 inhibits alkalosis-associated necrotic neuronal death by stimulating superoxide dismutase and catalase activity in immortalized mouse hypothalamic cells","volume":"1176","author":"Trubiani","year":"2007","journal-title":"Brain Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1016\/j.neuroscience.2012.05.069","article-title":"C-Terminal region of teneurin-1 co-localizes with dystroglycan and modulates cytoskeletal organization through an extracellular signal-regulated kinase-dependent stathmin- and filamin A-mediated mechanism in hippocampal cells","volume":"219","author":"Chand","year":"2012","journal-title":"Neuroscience"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"22","DOI":"10.3389\/fendo.2019.00022","article-title":"Teneurin C-Terminal Associated Peptide (TCAP)-1 and Latrophilin Interaction in HEK293 Cells: Evidence for Modulation of Intercellular Adhesion","volume":"10","author":"Husic","year":"2019","journal-title":"Front. Endocrinol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1241","DOI":"10.1016\/j.neuroscience.2006.09.062","article-title":"Regulation of neurite growth in immortalized mouse hypothalamic neurons and rat hippocampal primary cultures by teneurin C-terminal-associated peptide-1","volume":"144","author":"Belsham","year":"2007","journal-title":"Neuroscience"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"W98","DOI":"10.1093\/nar\/gkx247","article-title":"GEPIA: A web server for cancer and normal gene expression profiling and interactive analyses","volume":"45","author":"Tang","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1038\/ng.3275","article-title":"Transposon mutagenesis identifies genetic drivers of Braf(V600E) melanoma","volume":"47","author":"Mann","year":"2015","journal-title":"Nat. Genet."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1182\/bloodadvances.2017014118","article-title":"B-cell tumor development in Tet2-deficient mice","volume":"2","author":"Mouly","year":"2018","journal-title":"Blood Adv."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"22460","DOI":"10.18632\/oncotarget.25123","article-title":"Somatic mutations in early onset luminal breast cancer","volume":"9","author":"Encinas","year":"2018","journal-title":"Oncotarget"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"467","DOI":"10.21873\/cgp.20009","article-title":"A Comparative Study of the Molecular Characteristics of Familial Gliomas and Other Cancers","volume":"13","author":"Lu","year":"2016","journal-title":"Cancer Genomics Proteomics"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Petrini, I., Rajan, A., Pham, T., Voeller, D., Davis, S., Gao, J., Wang, Y., and Giaccone, G. (2013). Whole genome and transcriptome sequencing of a B3 thymoma. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0060572"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"4845","DOI":"10.1038\/onc.2014.406","article-title":"The landscape and therapeutic relevance of cancer-associated transcript fusions","volume":"34","author":"Yoshihara","year":"2015","journal-title":"Oncogene"},{"key":"ref_50","first-page":"D784","article-title":"ChimerDB 3.0: An enhanced database for fusion genes from cancer transcriptome and literature data mining","volume":"45","author":"Lee","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"15044","DOI":"10.1073\/pnas.251547398","article-title":"Gene expression in papillary thyroid carcinoma reveals highly consistent profiles","volume":"98","author":"Huang","year":"2001","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1007\/s10238-016-0445-y","article-title":"Overexpression of teneurin transmembrane protein 1 is a potential marker of disease progression in papillary thyroid carcinoma","volume":"17","author":"Cheng","year":"2017","journal-title":"Clin. Exp. Med."},{"key":"ref_53","first-page":"8429","article-title":"MicroRNA-486 inhibits cell proliferation, invasion and migration via down-regulating the TENM1 expressions and affecting ERK and Akt signaling pathways and epithelial-to-mesenchymal transition in papillary thyroid carcinoma","volume":"23","author":"Sun","year":"2019","journal-title":"Eur. Rev. Med. Pharmacol. Sci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1089\/thy.2016.0605","article-title":"Identification of Two Distinct Molecular Subtypes of Non-Invasive Follicular Neoplasm with Papillary-Like Nuclear Features by Digital RNA Counting","volume":"27","author":"Giannini","year":"2017","journal-title":"Thyroid"},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Wu, D., Hu, S., Hou, Y., He, Y., and Liu, S. (2020). Identification of potential novel biomarkers to differentiate malignant thyroid nodules with cytological indeterminate. BMC Cancer, 20.","DOI":"10.1186\/s12885-020-6676-z"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"113","DOI":"10.3892\/mmr.2014.2152","article-title":"Co-expression network analysis of differentially expressed genes associated with metastasis in prolactin pituaitary tumors","volume":"10","author":"Zhang","year":"2014","journal-title":"Mol. Med. Rep."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1733","DOI":"10.1038\/onc.2016.341","article-title":"ODZ1 allows glioblastoma to sustain invasiveness through a Myc-dependent transcriptional upregulation of RhoA","volume":"36","author":"Talamillo","year":"2017","journal-title":"Oncogene"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1036","DOI":"10.3389\/fonc.2019.01036","article-title":"Hypoxia Can Induce Migration of Glioblastoma Cells Through a Methylation-Dependent Control of ODZ1 Gene Expression","volume":"9","author":"Velasquez","year":"2019","journal-title":"Front. Oncol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"556","DOI":"10.1016\/j.stem.2012.03.009","article-title":"The PSA(-\/lo) prostate cancer cell population harbors self-renewing long-term tumor-propagating cells that resist castration","volume":"10","author":"Qin","year":"2012","journal-title":"Cell Stem Cell"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Tajima, T., Kito, F., Yoshida, A., Kawai, A., and Kondo, T. (2019). Calreticulin as A Novel Potential Metastasis-Associated Protein in Myxoid Liposarcoma, as Revealed by Two-Dimensional Difference Gel Electrophoresis. Proteomes, 7.","DOI":"10.3390\/proteomes7020013"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"21083","DOI":"10.1073\/pnas.1320659110","article-title":"Reproducible copy number variation patterns among single circulating tumor cells of lung cancer patients","volume":"110","author":"Ni","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Leamey, C.A., Merlin, S., Lattouf, P., Sawatari, A., Zhou, X., Demel, N., Glendining, K.A., Oohashi, T., Sur, M., and Fassler, R. (2007). Ten_m3 regulates eye-specific patterning in the mammalian visual pathway and is required for binocular vision. PLoS Biol., 5.","DOI":"10.1371\/journal.pbio.0050241"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"12490","DOI":"10.1523\/JNEUROSCI.4708-12.2013","article-title":"Ten-m2 is required for the generation of binocular visual circuits","volume":"33","author":"Young","year":"2013","journal-title":"J. NeuroSci."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Torres-da-Silva, K.R., Tessarin, G.W.L., Dias, C.A., Guiati, I.Z., Ervolino, E., Goncalves, A., Beneti, I.M., Lovejoy, D.A., and Casatti, C.A. (2017). Teneurin-2 presence in rat and human odontoblasts. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0184794"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.mce.2014.07.011","article-title":"Comparative gene array analysis of progenitor cells from human paired deep neck and subcutaneous adipose tissue","volume":"395","author":"Tews","year":"2014","journal-title":"Mol. Cell Endocrinol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1177\/117727190700200020","article-title":"Using LongSAGE to Detect Biomarkers of Cervical Cancer Potentially Amenable to Optical Contrast Agent Labelling","volume":"2","author":"Kneller","year":"2007","journal-title":"Biomark. Insights"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1159\/000091183","article-title":"A new specific gene expression in squamous cell carcinoma of the esophagus detected using representational difference analysis and cDNA microarray","volume":"70","author":"Kan","year":"2006","journal-title":"Oncology"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.lungcan.2011.07.009","article-title":"Proteomic surfaceome analysis of mesothelioma","volume":"75","author":"Ziegler","year":"2012","journal-title":"Lung Cancer"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"4340","DOI":"10.1038\/sj.onc.1208628","article-title":"Hepatitis B virus-related insertional mutagenesis in chronic hepatitis B patients as an early drastic genetic change leading to hepatocarcinogenesis","volume":"24","author":"Minami","year":"2005","journal-title":"Oncogene"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1016\/j.ccr.2005.10.001","article-title":"Integrative genomic and proteomic analysis of prostate cancer reveals signatures of metastatic progression","volume":"8","author":"Varambally","year":"2005","journal-title":"Cancer Cell"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.1158\/1078-0432.CCR-10-2320","article-title":"Involvement of the TGF-beta and beta-catenin pathways in pelvic lymph node metastasis in early-stage cervical cancer","volume":"17","author":"Noordhuis","year":"2011","journal-title":"Clin. Cancer Res."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"252","DOI":"10.2353\/ajpath.2007.061010","article-title":"Alterations of gene expression in the development of early hyperplastic precursors of breast cancer","volume":"171","author":"Lee","year":"2007","journal-title":"Am. J. Pathol."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Graumann, R., Di Capua, G.A., Oyarzun, J.E., Vasquez, M.A., Liao, C., Branes, J.A., Roa, I., Casanello, P., Corvalan, A.H., and Owen, G.I. (2017). Expression of teneurins is associated with tumor differentiation and patient survival in ovarian cancer. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0177244"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"809","DOI":"10.1677\/ERC-09-0326","article-title":"Prolactin and oestrogen synergistically regulate gene expression and proliferation of breast cancer cells","volume":"17","author":"Rasmussen","year":"2010","journal-title":"Endocr. Relat. Cancer"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"7113","DOI":"10.1002\/jcp.26634","article-title":"Genome-wide binding of transcription factor ZEB1 in triple-negative breast cancer cells","volume":"233","author":"Maturi","year":"2018","journal-title":"J. Cell Physiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1069","DOI":"10.1002\/gcc.20492","article-title":"Genetic changes in the evolution of multidrug resistance for cultured human ovarian cancer cells","volume":"46","author":"Buys","year":"2007","journal-title":"Genes Chromosomes Cancer"},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Mizuuchi, H., Suda, K., Sato, K., Tomida, S., Fujita, Y., Kobayashi, Y., Maehara, Y., Sekido, Y., Nishio, K., and Mitsudomi, T. (2015). Collateral chemoresistance to anti-microtubule agents in a lung cancer cell line with acquired resistance to erlotinib. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0123901"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"D920","DOI":"10.1093\/nar\/gks1082","article-title":"Atlas of genetics and cytogenetics in oncology and haematology in 2013","volume":"41","author":"Huret","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1038\/ng.2529","article-title":"The genetic landscape of high-risk neuroblastoma","volume":"45","author":"Pugh","year":"2013","journal-title":"Nat. Genet."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1038\/nature11154","article-title":"Sequence analysis of mutations and translocations across breast cancer subtypes","volume":"486","author":"Banerji","year":"2012","journal-title":"Nature"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1212","DOI":"10.4161\/cbt.7.8.6220","article-title":"Human breast cancer-associated fibroblasts (CAFs) show caveolin-1 downregulation and RB tumor suppressor functional inactivation: Implications for the response to hormonal therapy","volume":"7","author":"Mercier","year":"2008","journal-title":"Cancer Biol. Ther."},{"key":"ref_82","doi-asserted-by":"crossref","unstructured":"McGuire, T.F., Sajithlal, G.B., Lu, J., Nicholls, R.D., and Prochownik, E.V. (2012). In vivo evolution of tumor-derived endothelial cells. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0037138"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"580","DOI":"10.3389\/fnins.2019.00580","article-title":"Teneurins: Mediators of Complex Neural Circuit Assembly in Mammals","volume":"13","author":"Leamey","year":"2019","journal-title":"Front. Neurosci."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1016\/j.celrep.2013.09.045","article-title":"Teneurin-3 specifies morphological and functional connectivity of retinal ganglion cells in the vertebrate visual system","volume":"5","author":"Antinucci","year":"2013","journal-title":"Cell Rep."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1006\/geno.1999.5798","article-title":"Mapping homologs of Drosophila odd Oz (odz): Doc4\/Odz4 to mouse chromosome 7, Odz1 to mouse chromosome 11; and ODZ3 to human chromosome Xq25","volume":"58","author":"Wides","year":"1999","journal-title":"Genomics"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"505","DOI":"10.3389\/fnins.2019.00505","article-title":"Wnt Signaling Upregulates Teneurin-3 Expression via Canonical and Non-canonical Wnt Pathway Crosstalk","volume":"13","author":"Martinez","year":"2019","journal-title":"Front. Neurosci."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"792","DOI":"10.1002\/ijc.31104","article-title":"The human PKP2\/plakophilin-2 gene is induced by Wnt\/beta-catenin in normal and colon cancer-associated fibroblasts","volume":"142","author":"Niell","year":"2018","journal-title":"Int. J. Cancer"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"1079","DOI":"10.1038\/s41467-018-03460-0","article-title":"Structures of Teneurin adhesion receptors reveal an ancient fold for cell-cell interaction","volume":"9","author":"Jackson","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/j.pbiomolbio.2013.02.002","article-title":"Systems approaches to genomic and epigenetic inter-regulation of peptide hormones in stress and reproduction","volume":"113","author":"Lovejoy","year":"2013","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"194","DOI":"10.3389\/fonc.2012.00194","article-title":"Identification of cell surface proteins as potential immunotherapy targets in 12 pediatric cancers","volume":"2","author":"Orentas","year":"2012","journal-title":"Front. Oncol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"3791","DOI":"10.1021\/pr800964v","article-title":"Comprehensive profiling of the cell surface proteome of Sy5Y neuroblastoma cells yields a subset of proteins associated with tumor differentiation","volume":"8","author":"Garcia","year":"2009","journal-title":"J. Proteome Res."},{"key":"ref_92","first-page":"399","article-title":"Genomic signature induced by pregnancy in the human breast","volume":"28","author":"Balogh","year":"2006","journal-title":"Int. J. Oncol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"931s","DOI":"10.1158\/1078-0432.931s.11.2","article-title":"Breast differentiation and its implication in cancer prevention","volume":"11 Pt 2","author":"Russo","year":"2005","journal-title":"Clin. Cancer Res."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"2587","DOI":"10.4161\/15384101.2015.942210","article-title":"Indole-3-carbinol and its N-alkoxy derivatives preferentially target ERalpha-positive breast cancer cells","volume":"13","author":"Caruso","year":"2014","journal-title":"Cell Cycle"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"1315","DOI":"10.1016\/j.cell.2009.11.025","article-title":"Tumor self-seeding by circulating cancer cells","volume":"139","author":"Kim","year":"2009","journal-title":"Cell"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"1986","DOI":"10.1016\/j.jprot.2010.06.003","article-title":"Novel post-digest isotope coded protein labeling method for phospho- and glycoproteome analysis","volume":"73","author":"Fleron","year":"2010","journal-title":"J. Proteomics"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"e4109","DOI":"10.1097\/MD.0000000000004109","article-title":"Integrative radiogenomic analysis for genomic signatures in glioblastomas presenting leptomeningeal dissemination","volume":"95","author":"You","year":"2016","journal-title":"Medicine"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1038\/nature10910","article-title":"Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes","volume":"483","author":"Molenaar","year":"2012","journal-title":"Nature"},{"key":"ref_99","doi-asserted-by":"crossref","unstructured":"Jang, M.K., Shen, K., and McBride, A.A. (2014). Papillomavirus genomes associate with BRD4 to replicate at fragile sites in the host genome. PLoS Pathog., 10.","DOI":"10.1371\/journal.ppat.1004117"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1111\/bpa.12295","article-title":"Epithelioid Glioblastomas and Anaplastic Epithelioid Pleomorphic Xanthoastrocytomas--Same Entity or First Cousins?","volume":"26","author":"Alexandrescu","year":"2016","journal-title":"Brain Pathol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"68270","DOI":"10.18632\/oncotarget.11392","article-title":"Association mining of mutated cancer genes in different clinical stages across 11 cancer types","volume":"7","author":"Hu","year":"2016","journal-title":"Oncotarget"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1171","DOI":"10.1093\/jnci\/djy168","article-title":"Effect Sizes of Somatic Mutations in Cancer","volume":"110","author":"Cannataro","year":"2018","journal-title":"J. Natl. Cancer Inst."},{"key":"ref_103","doi-asserted-by":"crossref","unstructured":"Tanyi, J.L., Bobisse, S., Ophir, E., Tuyaerts, S., Roberti, A., Genolet, R., Baumgartner, P., Stevenson, B.J., Iseli, C., and Dangaj, D. (2018). Personalized cancer vaccine effectively mobilizes antitumor T cell immunity in ovarian cancer. Sci. Transl. Med., 10.","DOI":"10.1126\/scitranslmed.aao5931"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"3055","DOI":"10.1242\/dev.01885","article-title":"Comparative analysis of genes downstream of the Hoxd cluster in developing digits and external genitalia","volume":"132","author":"Cobb","year":"2005","journal-title":"Development"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"1386","DOI":"10.1096\/fj.13-241034","article-title":"Teneurin-4 promotes cellular protrusion formation and neurite outgrowth through focal adhesion kinase signaling","volume":"28","author":"Suzuki","year":"2014","journal-title":"FASEB J."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"11586","DOI":"10.1523\/JNEUROSCI.2045-11.2012","article-title":"Teneurin-4 is a novel regulator of oligodendrocyte differentiation and myelination of small-diameter axons in the CNS","volume":"32","author":"Suzuki","year":"2012","journal-title":"J. Neurosci."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"5677","DOI":"10.1093\/hmg\/ddv281","article-title":"Missense mutations in TENM4, a regulator of axon guidance and central myelination, cause essential tremor","volume":"24","author":"Hor","year":"2015","journal-title":"Hum. Mol. Genet."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1002\/mds.26753","article-title":"Teneurin transmembrane protein 4 is not a cause for essential tremor in a Canadian population","volume":"32","author":"Houle","year":"2017","journal-title":"Mov. Disord."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"915","DOI":"10.1002\/jor.22616","article-title":"Teneurin-4, a transmembrane protein, is a novel regulator that suppresses chondrogenic differentiation","volume":"32","author":"Suzuki","year":"2014","journal-title":"J. Orthop. Res."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/j.devcel.2012.07.014","article-title":"Colonization of the satellite cell niche by skeletal muscle progenitor cells depends on Notch signals","volume":"23","author":"Brohl","year":"2012","journal-title":"Dev. Cell"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"3017","DOI":"10.1002\/stem.2058","article-title":"Muscle Satellite Cell Protein Teneurin-4 Regulates Differentiation During Muscle Regeneration","volume":"33","author":"Ishii","year":"2015","journal-title":"Stem Cells"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"499","DOI":"10.3109\/10253890802666112","article-title":"Expression quantitative trait loci and genetic regulatory network analysis reveals that Gabra2 is involved in stress responses in the mouse","volume":"12","author":"Dai","year":"2009","journal-title":"Stress"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"e1700429","DOI":"10.1002\/biot.201700429","article-title":"Multiplexed Digital mRNA Expression Analysis Profiles System-Wide Changes in mRNA Abundance and Responsiveness of UPR-Specific Gene Expression Changes during Batch Culture of Recombinant Chinese Hamster Ovary Cells","volume":"13","author":"Dickson","year":"2018","journal-title":"Biotechnol. J."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"e154","DOI":"10.1038\/tp.2012.80","article-title":"Epistasis network centrality analysis yields pathway replication across two GWAS cohorts for bipolar disorder","volume":"2","author":"Pandey","year":"2012","journal-title":"Transl. Psychiatry"},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1016\/j.schres.2014.07.004","article-title":"Replication of previous genome-wide association studies of psychiatric diseases in a large schizophrenia case-control sample from Spain","volume":"159","author":"Ivorra","year":"2014","journal-title":"Schizophr. Res."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"725","DOI":"10.3389\/fgene.2018.00725","article-title":"Exome Sequencing Identifies TENM4 as a Novel Candidate Gene for Schizophrenia in the SCZD2 Locus at 11q14-21","volume":"9","author":"Xue","year":"2018","journal-title":"Front. Genet."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1111\/bdi.12068","article-title":"The risk variant in ODZ4 for bipolar disorder impacts on amygdala activation during reward processing","volume":"15","author":"Heinrich","year":"2013","journal-title":"Bipolar Disord."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"1337","DOI":"10.4088\/JCP.15m10314","article-title":"Genetic Risk Score Analysis in Early-Onset Bipolar Disorder","volume":"78","author":"Croarkin","year":"2017","journal-title":"J. Clin. Psychiatry"},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"41237","DOI":"10.18632\/oncotarget.5652","article-title":"Novel insights into Notum and glypicans regulation in colorectal cancer","volume":"6","author":"Arigoni","year":"2015","journal-title":"Oncotarget"},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"101386","DOI":"10.1016\/j.smim.2020.101386","article-title":"Breast cancer stem cell antigens as targets for immunotherapy","volume":"47","author":"Quaglino","year":"2020","journal-title":"Semin. Immunol."},{"key":"ref_121","doi-asserted-by":"crossref","unstructured":"Ruiu, R., Barutello, G., Arigoni, M., Riccardo, F., Conti, L., Peppino, G., Annaratone, L., Marchi\u00f2, C., Mengozzi, G., and Calogero, R.A. (2021). Identification of TENM4 as a Novel Cancer Stem Cell-Associated Molecule and Potential Target in Triple Negative Breast Cancer. Cancers, 13.","DOI":"10.3390\/cancers13040894"},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"5718","DOI":"10.1038\/sj.onc.1202950","article-title":"gamma-heregulin is the product of a chromosomal translocation fusing the DOC4 and HGL\/NRG1 genes in the MDA-MB-175 breast cancer cell line","volume":"18","author":"Wang","year":"1999","journal-title":"Oncogene"},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"7110","DOI":"10.1038\/sj.onc.1203136","article-title":"Gamma-heregulin: A fusion gene of DOC-4 and neuregulin-1 derived from a chromosome translocation","volume":"18","author":"Liu","year":"1999","journal-title":"Oncogene"},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"1385","DOI":"10.1038\/sj.onc.1201317","article-title":"Gamma-heregulin: A novel heregulin isoform that is an autocrine growth factor for the human breast cancer cell line, MDA-MB-175","volume":"15","author":"Schaefer","year":"1997","journal-title":"Oncogene"},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"1205","DOI":"10.1126\/science.256.5060.1205","article-title":"Identification of heregulin, a specific activator of p185erbB2","volume":"256","author":"Holmes","year":"1992","journal-title":"Science"},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1038\/nature14664","article-title":"Comprehensive genomic profiles of small cell lung cancer","volume":"524","author":"George","year":"2015","journal-title":"Nature"},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1038\/nature14666","article-title":"Non-coding recurrent mutations in chronic lymphocytic leukaemia","volume":"526","author":"Puente","year":"2015","journal-title":"Nature"},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"2734","DOI":"10.1021\/pr2003038","article-title":"A comprehensive map of the human urinary proteome","volume":"10","author":"Marimuthu","year":"2011","journal-title":"J. Proteome Res."},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"11175","DOI":"10.18632\/oncotarget.3579","article-title":"Inhibition of cathepsin proteases attenuates migration and sensitizes aggressive N-Myc amplified human neuroblastoma cells to doxorubicin","volume":"6","author":"Gangoda","year":"2015","journal-title":"Oncotarget"},{"key":"ref_130","doi-asserted-by":"crossref","first-page":"15375","DOI":"10.18632\/oncotarget.3801","article-title":"Proteogenomic analysis reveals exosomes are more oncogenic than ectosomes","volume":"6","author":"Keerthikumar","year":"2015","journal-title":"Oncotarget"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/5\/2321\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:28:57Z","timestamp":1760160537000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/5\/2321"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,2,26]]},"references-count":130,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2021,3]]}},"alternative-id":["ijms22052321"],"URL":"https:\/\/doi.org\/10.3390\/ijms22052321","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,2,26]]}}}