{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,10]],"date-time":"2026-11-10T21:01:10Z","timestamp":1794344470307,"version":"4.9.0"},"reference-count":60,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2021,4,8]],"date-time":"2021-04-08T00:00:00Z","timestamp":1617840000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Diagnostics"],"abstract":"<jats:p>The C-Maf-Inducing protein (CMIP) was first described as overexpressed in T cell subpopulations of idiopathic nephrotic syndrome (INS) patients. Later, it was found concomitantly upregulated in podocytes. CMIP expression has also been reported in several types of cancer, including blood malignancies and solid tumors, in many cases accompanied by nephrotic syndrome. In addition to these observations, the duality of CMIP overexpression in the kidney and INS lesions, has been extensively reported as one of the adverse effects of anticancer therapy based on anti-receptor tyrosine kinase drugs. As a consequence, a growing body of evidence points at CMIP as playing a role in cancer. This includes its reciprocal regulatory ties with NF-\u03baB and WT1, and the more recent reports showing an involvement in regulatory circuits in cancer cells. The ensemble of the current information justifies to propose CMIP as an important piece of the puzzle of biological systems involved in cancer and other diseases and its potential as a target.<\/jats:p>","DOI":"10.3390\/diagnostics11040666","type":"journal-article","created":{"date-parts":[[2021,4,8]],"date-time":"2021-04-08T10:34:39Z","timestamp":1617878079000},"page":"666","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["The Enigmatic Emerging Role of the C-Maf Inducing Protein in Cancer"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3590-706X","authenticated-orcid":false,"given":"Mario","family":"Ollero","sequence":"first","affiliation":[{"name":"Univ Paris Est Creteil, INSERM, IMRB, F-94010 Creteil, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3663-4470","authenticated-orcid":false,"given":"Dil","family":"Sahali","sequence":"additional","affiliation":[{"name":"Univ Paris Est Creteil, INSERM, IMRB, F-94010 Creteil, France"},{"name":"AP-HP, Hopital Henri Mondor, Service N\u00e9phrologie, F-94010 Creteil, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,4,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1681\/ASN.V1351238","article-title":"A novel approach to investigation of the pathogenesis of active minimal-change nephrotic syndrome using subtracted cDNA library screening","volume":"13","author":"Sahali","year":"2002","journal-title":"J. Am. Soc. Nephrol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1084\/jem.20030566","article-title":"Truncation of C-mip (Tc-mip), a new proximal signaling protein, induces c-maf Th2 transcription factor and cytoskeleton reorganization","volume":"198","author":"Grimbert","year":"2003","journal-title":"J. Exp. Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1093\/dnares\/7.6.347","article-title":"Prediction of the coding sequences of unidentified human genes. XIX. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro","volume":"7","author":"Nagase","year":"2000","journal-title":"DNA Res."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1016\/j.ajhg.2009.07.004","article-title":"CMIP and ATP2C2 modulate phonological short-term memory in language impairment","volume":"85","author":"Newbury","year":"2009","journal-title":"Am. J. Hum. Genet."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1298","DOI":"10.1016\/j.kint.2016.07.016","article-title":"Repression of CMIP transcription by WT1 is relevant to podocyte health","volume":"90","author":"Moktefi","year":"2016","journal-title":"Kidney Int."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.jaut.2017.10.006","article-title":"NEPHRUTIX: A randomized, double-blind, placebo vs Rituximab-controlled trial assessing T-cell subset changes in Minimal Change Nephrotic Syndrome","volume":"88","author":"Boumediene","year":"2018","journal-title":"J. Autoimmun."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"ra39","DOI":"10.1126\/scisignal.2000678","article-title":"c-mip impairs podocyte proximal signaling and induces heavy proteinuria","volume":"3","author":"Zhang","year":"2010","journal-title":"Sci. Signal."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1038\/ki.2012.426","article-title":"Upregulation of c-mip is closely related to podocyte dysfunction in membranous nephropathy","volume":"83","author":"Sendeyo","year":"2013","journal-title":"Kidney Int."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Bouachi, K., Moktefi, A., Zhang, S.Y., Oniszczuk, J., Sendeyo, K., Remy, P., Audard, V., Pawlak, A., Ollero, M., and Sahali, D. (2018). Expression of CMIP in podocytes is restricted to specific classes of lupus nephritis. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0207066"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1274","DOI":"10.1159\/000430296","article-title":"Induction of C-Mip by IL-17 Plays an Important Role in Adriamycin-Induced Podocyte Damage","volume":"36","author":"Liu","year":"2015","journal-title":"Cell. Physiol. Biochem."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1016\/j.molimm.2008.09.034","article-title":"C-mip interacts physically with RelA and inhibits nuclear factor kappa B activity","volume":"46","author":"Kamal","year":"2009","journal-title":"Mol. Immunol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1257","DOI":"10.1016\/j.molimm.2003.11.035","article-title":"The Filamin-A is a partner of Tc-mip, a new adapter protein involved in c-maf-dependent Th2 signaling pathway","volume":"40","author":"Grimbert","year":"2004","journal-title":"Mol. Immunol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1016\/j.febslet.2009.12.015","article-title":"C-mip interacts with the p85 subunit of PI3 kinase and exerts a dual effect on ERK signaling via the recruitment of Dip1 and DAP kinase","volume":"584","author":"Kamal","year":"2010","journal-title":"FEBS Lett."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"3756","DOI":"10.1182\/blood-2009-11-251132","article-title":"Occurrence of minimal change nephrotic syndrome in classical Hodgkin lymphoma is closely related to the induction of c-mip in Hodgkin-Reed Sternberg cells and podocytes","volume":"115","author":"Audard","year":"2010","journal-title":"Blood"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1016\/j.cellsig.2012.11.017","article-title":"Inhibition of nephrin activation by c-mip through Csk-Cbp-Fyn axis plays a critical role in Angiotensin II-induced podocyte damage","volume":"25","author":"Yu","year":"2013","journal-title":"Cell. Signal."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Oniszczuk, J., Sendeyo, K., Chhuon, C., Savas, B., Cogne, E., Vachin, P., Henique, C., Guerrera, I.C., Astarita, G., and Frontera, V. (2020). CMIP is a negative regulator of T cell signaling. Cell. Mol. Immunol.","DOI":"10.1038\/s41423-019-0266-5"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4955","DOI":"10.3892\/mmr.2017.7156","article-title":"cMaf inducing protein inhibits cofilin1 activity and alters podocyte cytoskeleton organization","volume":"16","author":"Yu","year":"2017","journal-title":"Mol. Med. Rep."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"433","DOI":"10.2337\/db15-0828","article-title":"Numerous Genes in Loci Associated with Body Fat Distribution Are Linked to Adipose Function","volume":"65","author":"Dahlman","year":"2016","journal-title":"Diabetes"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1161\/ATVBAHA.116.308831","article-title":"DNA Methylation and High-Density Lipoprotein Functionality-Brief Report: The REGICOR Study (Registre Gironi del Cor)","volume":"37","author":"Hernaez","year":"2017","journal-title":"Arterioscler. Thromb. Vasc. Biol."},{"key":"ref_20","first-page":"443","article-title":"Association between obesity and DNA methylation among the 7-16 year-old twins","volume":"39","author":"Li","year":"2018","journal-title":"Zhonghua Liu Xing Bing Xue Za Zhi"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1357","DOI":"10.4049\/jimmunol.1601157","article-title":"The MHC Class II Immunopeptidome of Lymph Nodes in Health and in Chemically Induced Colitis","volume":"198","author":"Fugmann","year":"2017","journal-title":"J. Immunol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1002\/gepi.22126","article-title":"Genome-wide interaction with the insulin secretion locus MTNR1B reveals CMIP as a novel type 2 diabetes susceptibility gene in African Americans","volume":"42","author":"Keaton","year":"2018","journal-title":"Genet. Epidemiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1007\/s00592-018-1168-1","article-title":"Association analysis of copy number variations in type 2 diabetes-related susceptible genes in a Chinese population","volume":"55","author":"Yan","year":"2018","journal-title":"Acta Diabetol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1038\/ng.1019","article-title":"Meta-analysis of genome-wide association studies identifies eight new loci for type 2 diabetes in east Asians","volume":"44","author":"Cho","year":"2012","journal-title":"Nat. Genet."},{"key":"ref_25","first-page":"159","article-title":"East Asian Genome-wide association study derived loci in relation to type 2 diabetes in the Han Chinese population","volume":"66","author":"Zhang","year":"2019","journal-title":"Acta Biochim. Pol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Sakai, K., Imamura, M., Tanaka, Y., Iwata, M., Hirose, H., Kaku, K., Maegawa, H., Watada, H., Tobe, K., and Kashiwagi, A. (2013). Replication study for the association of 9 East Asian GWAS-derived loci with susceptibility to type 2 diabetes in a Japanese population. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0076317"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Cao, Y., Wang, T., Wu, Y., Juan, J., Qin, X., Tang, X., Wu, T., and Hu, Y. (2018). Opposite Genetic Effects of CMIP Polymorphisms on the Risk of Type 2 Diabetes and Obesity: A Family-Based Study in China. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19041011"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1108","DOI":"10.1093\/hmg\/ddt488","article-title":"A meta-analysis of genome-wide association studies for adiponectin levels in East Asians identifies a novel locus near WDR11-FGFR2","volume":"23","author":"Wu","year":"2014","journal-title":"Hum. Mol. Genet."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1016\/j.ebiom.2018.05.033","article-title":"Loss of Cardio-Protective Effects at the CDH13 Locus Due to Gene-Sleep Interaction: The BCAMS Study","volume":"32","author":"Li","year":"2018","journal-title":"EBioMedicine"},{"key":"ref_30","unstructured":"Benitez-Burraco, A., Fernandez-Urquiza, M., and Jimenez-Romero, S. (2016). Language impairment with a microduplication in 1q42.3q43. Clin. Linguist. Phon., 1\u201326."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.bandl.2014.03.007","article-title":"Human speech- and reading-related genes display partially overlapping expression patterns in the marmoset brain","volume":"133","author":"Kato","year":"2014","journal-title":"Brain Lang."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"3381","DOI":"10.1044\/2019_JSLHR-L-19-0001","article-title":"Using Polygenic Profiles to Predict Variation in Language and Psychosocial Outcomes in Early and Middle Childhood","volume":"62","author":"Newbury","year":"2019","journal-title":"J. Speech Lang. Hear. Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1002\/aur.1436","article-title":"Language impairment and dyslexia genes influence language skills in children with autism spectrum disorders","volume":"8","author":"Eicher","year":"2015","journal-title":"Autism Res."},{"key":"ref_34","first-page":"574","article-title":"Differentially expressed genes identified in the main olfactory epithelium of mice with deficiency of adenylate cyclase 3 by using suppression subtractive hybridization approach","volume":"36","author":"Zhenlong","year":"2014","journal-title":"Yi Chuan"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Pan, L., Liao, Y.H., Mo, M.Q., Zhang, Q.H., and Yin, R.X. (2020). CMIP SNPs and their haplotypes are associated with dyslipidaemia and clinicopathologic features of IgA nephropathy. Biosci. Rep., 40.","DOI":"10.1042\/BSR20202628"},{"key":"ref_36","first-page":"5008","article-title":"The association of the CMIP rs16955379 polymorphism with dyslipidemia and the clinicopathological features of IgA nephropathy","volume":"11","author":"Mo","year":"2018","journal-title":"Int. J. Clin. Exp. Pathol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Bryant, E.K., Dressen, A.S., Bunker, C.H., Hokanson, J.E., Hamman, R.F., Kamboh, M.I., and Demirci, F.Y. (2013). A multiethnic replication study of plasma lipoprotein levels-associated SNPs identified in recent GWAS. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0063469"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Strawbridge, R.J., Laumen, H., Hamsten, A., Breier, M., Grallert, H., Hauner, H., Arner, P., and Dahlman, I. (2016). Effects of Genetic Loci Associated with Central Obesity on Adipocyte Lipolysis. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0153990"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2101","DOI":"10.1002\/ajmg.a.38277","article-title":"CMIP haploinsufficiency in two patients with autism spectrum disorder and co-occurring gastrointestinal issues","volume":"173","author":"Luo","year":"2017","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2251","DOI":"10.1038\/sj.ki.5000341","article-title":"Minimal change nephrotic syndrome and classical Hodgkin\u2019s lymphoma: Report of 21 cases and review of the literature","volume":"69","author":"Audard","year":"2006","journal-title":"Kidney Int."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1053\/j.ajkd.2016.09.026","article-title":"Nephrotic Syndrome in Small Cell Lung Cancer and Induction of C-Mip in Podocytes","volume":"69","author":"Bouatou","year":"2017","journal-title":"Am. J. Kidney Dis."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"7277","DOI":"10.3892\/mmr.2017.7541","article-title":"CMIP is oncogenic in human gastric cancer cells","volume":"16","author":"Zhang","year":"2017","journal-title":"Mol. Med. Rep."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"152776","DOI":"10.1016\/j.prp.2019.152776","article-title":"CMIP promotes Herceptin resistance of HER2 positive gastric cancer cells","volume":"216","author":"Xiang","year":"2020","journal-title":"Pathol. Res. Pract."},{"key":"ref_44","first-page":"5340160","article-title":"CMIP Promotes Proliferation and Metastasis in Human Glioma","volume":"2017","author":"Wang","year":"2017","journal-title":"Biomed. Res. Int."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/j.jaad.2014.04.042","article-title":"Development of a novel noninvasive adhesive patch test for the evaluation of pigmented lesions of the skin","volume":"71","author":"Gerami","year":"2014","journal-title":"J. Am. Acad. Dermatol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.placenta.2020.02.009","article-title":"Differential placental methylation in preeclampsia, preterm and term pregnancies","volume":"93","author":"Li","year":"2020","journal-title":"Placenta"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"3238","DOI":"10.1158\/0008-5472.CAN-14-0013","article-title":"Colorectal cancer cell lines are representative models of the main molecular subtypes of primary cancer","volume":"74","author":"Mouradov","year":"2014","journal-title":"Cancer Res."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Wang, C.C.N., Li, C.Y., Cai, J.H., Sheu, P.C., Tsai, J.J.P., Wu, M.Y., Li, C.J., and Hou, M.F. (2019). Identification of Prognostic Candidate Genes in Breast Cancer by Integrated Bioinformatic Analysis. J. Clin. Med., 8.","DOI":"10.3390\/jcm8081160"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1038\/ki.2013.344","article-title":"Expression patterns of RelA and c-mip are associated with different glomerular diseases following anti-VEGF therapy","volume":"85","author":"Izzedine","year":"2014","journal-title":"Kidney Int."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1449","DOI":"10.1093\/ndt\/gfu368","article-title":"Inhibition of the VEGF signalling pathway and glomerular disorders","volume":"30","author":"Ollero","year":"2015","journal-title":"Nephrol. Dial. Transplant."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1186\/s12935-020-01258-z","article-title":"FOXC1-induced LINC01123 acts as a mediator in triple negative breast cancer","volume":"20","author":"Zhang","year":"2020","journal-title":"Cancer Cell Int."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"F12","DOI":"10.1152\/ajprenal.00597.2007","article-title":"New insights into the function of the Wilms tumor suppressor gene WT1 in podocytes","volume":"295","author":"Morrison","year":"2008","journal-title":"Am. J. Physiol. Renal Physiol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1017\/S1462399407000336","article-title":"The role of the Wilms tumour gene (WT1) in normal and malignant haematopoiesis","volume":"9","author":"Ariyaratana","year":"2007","journal-title":"Expert Rev. Mol. Med."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/j.bcp.2019.05.016","article-title":"Magnesium isoglycyrrhizinate ameliorates fructose-induced podocyte apoptosis through downregulation of miR-193a to increase WT1","volume":"166","author":"Li","year":"2019","journal-title":"Biochem. Pharmacol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"2284","DOI":"10.1016\/j.ajpath.2012.02.008","article-title":"c-mip down-regulates NF-kappaB activity and promotes apoptosis in podocytes","volume":"180","author":"Ory","year":"2012","journal-title":"Am. J. Pathol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1542","DOI":"10.1016\/j.bbalip.2013.03.001","article-title":"Emerging roles of lipids in BCL-2 family-regulated apoptosis","volume":"1831","author":"Zhang","year":"2013","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Li, G., Kidd, J., Kaspar, C., Dempsey, S., Bhat, O.M., Camus, S., Ritter, J.K., Gehr, T.W.B., Gulbins, E., and Li, P.L. (2020). Podocytopathy and Nephrotic Syndrome in Mice with Podocyte-Specific Deletion of the Asah1 Gene: Role of Ceramide Accumulation in Glomeruli. Am. J. Pathol.","DOI":"10.1016\/j.ajpath.2020.02.008"},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Cancer Genome Atlas Network (2012). Comprehensive molecular characterization of human colon and rectal cancer. Nature, 487, 330\u2013337.","DOI":"10.1038\/nature11252"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1093\/hmg\/ddn322","article-title":"Transcript- and tissue-specific imprinting of a tumour suppressor gene","volume":"18","author":"Schulz","year":"2009","journal-title":"Hum. Mol. Genet."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1007\/s11010-006-9332-2","article-title":"Overexpression of BLCAP induces S phase arrest and apoptosis independent of p53 and NF-kappaB in human tongue carcinoma: BLCAP overexpression induces S phase arrest and apoptosis","volume":"297","author":"Yao","year":"2007","journal-title":"Mol. Cell. Biochem."}],"container-title":["Diagnostics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4418\/11\/4\/666\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T13:26:36Z","timestamp":1760361996000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4418\/11\/4\/666"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,8]]},"references-count":60,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2021,4]]}},"alternative-id":["diagnostics11040666"],"URL":"https:\/\/doi.org\/10.3390\/diagnostics11040666","relation":{},"ISSN":["2075-4418"],"issn-type":[{"value":"2075-4418","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,4,8]]}}}