{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,14]],"date-time":"2026-09-14T22:24:13Z","timestamp":1789424653299,"version":"build-2803163510"},"reference-count":38,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2017,2,10]],"date-time":"2017-02-10T00:00:00Z","timestamp":1486684800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Training Program of the Major Research Plan of the National Natural Science Foundation of China","award":["91543132"],"award-info":[{"award-number":["91543132"]}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["30901249, 81101267, 81541070"],"award-info":[{"award-number":["30901249, 81101267, 81541070"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003453","name":"Guangdong Natural Science Foundation","doi-asserted-by":"publisher","award":["10151063201000036,S2011010002526and 2016A030313089"],"award-info":[{"award-number":["10151063201000036,S2011010002526and 2016A030313089"]}],"id":[{"id":"10.13039\/501100003453","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003785","name":"Guangdong Province Medical Research Foundation","doi-asserted-by":"publisher","award":["A2014374, A2015310"],"award-info":[{"award-number":["A2014374, A2015310"]}],"id":[{"id":"10.13039\/501100003785","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Project from Jinan university","award":["21612426, 21615426, JNUPHPM2016001, JNUPHPM2016002"],"award-info":[{"award-number":["21612426, 21615426, JNUPHPM2016001, JNUPHPM2016002"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Background: Lipoma preferred partner (LPP) and T-cell activation Rho GTPase activating protein (TAGAP) polymorphisms might influence the susceptibility to celiac disease. Therefore, we performed a meta-analysis by identifying relevant studies to estimate the risks of these polymorphisms on celiac disease. Methods: The PubMed, Web of Science and Embase databases were searched (up to October 2016) for LPP rs1464510 and TAGAP rs1738074 polymorphisms. Results: This meta-analysis included the same 7 studies for LPP rs1464510 and TAGAP rs1738074. The minor risk A allele at both rs1464510 and rs1738074 carried risks (odds ratios) of 1.26 (95% CI: 1.22\u20131.30) and 1.17 (95% CI: 1.14\u20131.21), respectively, which contributed to increased risks in all celiac disease patients by 10.72% and 6.59%, respectively. The estimated lambdas were 0.512 and 0.496, respectively, suggesting that a co-dominant model would be suitable for both gene effects. Conclusions: This meta-analysis provides robust estimates that polymorphisms in LPP and TAGAP genes are potential risk factors for celiac disease in European and American. Prospective studies and more genome-wide association studies (GWAS) are needed to confirm these findings, and some corresponding molecular biology experiments should be carried out to clarify the pathogenic mechanisms of celiac disease.<\/jats:p>","DOI":"10.3390\/ijerph14020171","type":"journal-article","created":{"date-parts":[[2017,2,10]],"date-time":"2017-02-10T05:27:09Z","timestamp":1486704429000},"page":"171","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Association of LPP and TAGAP Polymorphisms with Celiac Disease Risk: A Meta-Analysis"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5320-1429","authenticated-orcid":false,"given":"Shi-Qi","family":"Huang","sequence":"first","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Na","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"},{"name":"Department of Preventive Medicine, Zunyi Medical College, Zhuhai Campus, Zhuhai 519041, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2180-6471","authenticated-orcid":false,"given":"Zi-Xing","family":"Zhou","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chui-Can","family":"Huang","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cheng-Li","family":"Zeng","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Di","family":"Xiao","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cong-Cong","family":"Guo","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ya-Jing","family":"Han","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiao-Hong","family":"Ye","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xing-Guang","family":"Ye","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mei-Ling","family":"Ou","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bao-Huan","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eddy","family":"Zeng","sequence":"additional","affiliation":[{"name":"School of Environment, Guangzhou Key Laboratory of Environmental Exposure and Health, Guangdong Key Laboratory of Environmental Pollution and Health, Jinan University, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guang","family":"Yang","sequence":"additional","affiliation":[{"name":"School of Environment, Guangzhou Key Laboratory of Environmental Exposure and Health, Guangdong Key Laboratory of Environmental Pollution and Health, Jinan University, Guangzhou 510632, Guangdong, China"},{"name":"Department of Parasitology, School of Basic Medical Sciences, Jinan University, Guangzhou 510632, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7333-4181","authenticated-orcid":false,"given":"Chun-Xia","family":"Jing","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, School of Basic Medical Sciences, Jinan University, No.601 Huangpu Road West, Guangzhou 510632, Guangdong, China"},{"name":"School of Environment, Guangzhou Key Laboratory of Environmental Exposure and Health, Guangdong Key Laboratory of Environmental Pollution 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Pediatr. Gastroenterol. Nutr."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1111\/j.1651-2227.1955.tb04269.x","article-title":"Coeliac disease. V. Some experiments on the cause of the harmful effect of wheat gliadin","volume":"44","author":"Weijers","year":"1955","journal-title":"Acta Paediatr."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1038\/nri885","article-title":"Coeliac disease: Dissecting a complex inflammatory disorder","volume":"2","author":"Sollid","year":"2002","journal-title":"Nat. Rev. Immunol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"738","DOI":"10.1053\/j.gastro.2007.11.041","article-title":"Combined functional and positional gene information for the identification of susceptibility variants in celiac disease","volume":"134","author":"Hualde","year":"2008","journal-title":"Gastroenterology"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/j.bpg.2005.01.001","article-title":"Genetics in coeliac disease","volume":"19","author":"Hunt","year":"2005","journal-title":"Best Pract. Res. Clin. Gastroenterol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1136\/jmg.2011.089714","article-title":"Revisiting genome wide association studies (GWAS) in coeliac disease: Replication study in spanish population and expression analysis of candidate genes","volume":"48","author":"Irastorza","year":"2011","journal-title":"J. Med. Genet."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1038\/ng.543","article-title":"Multiple common variants for celiac disease influencing immune gene expression","volume":"42","author":"Dubois","year":"2010","journal-title":"Nat. Genet."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1038\/ng.102","article-title":"Newly identified genetic risk variants for celiac disease related to the immune response","volume":"40","author":"Hunt","year":"2008","journal-title":"Nat. Genet."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1038\/ng2058","article-title":"A genome-wide association study for celiac disease identifies risk variants in the region harboring IL2 and IL21","volume":"39","author":"Franke","year":"2007","journal-title":"Nat. Genet."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1038\/gene.2011.8","article-title":"Fine mapping the TAGAP risk locus in rheumatoid arthritis","volume":"12","author":"Chen","year":"2011","journal-title":"Genes Immun."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Festen, E.A., Goyette, P., Green, T., Boucher, G., Beauchamp, C., Trynka, G., Dubois, P.C., Lagace, C., Stokkers, P.C., and Hommes, D.W. (2011). A meta-analysis of genome-wide association scans identifies IL18RAP, PTPN2, TAGAP, and PUS10 as shared risk loci for Crohn\u2019s disease and celiac disease. PLoS Genet., 7.","DOI":"10.1371\/journal.pgen.1001283"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2767","DOI":"10.1056\/NEJMoa0807917","article-title":"Shared and distinct genetic variants in type 1 diabetes and celiac disease","volume":"359","author":"Smyth","year":"2008","journal-title":"N. Engl. J. Med."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Eyre, S., Hinks, A., Bowes, J., Flynn, E., Martin, P., Wilson, A.G., Morgan, A.W., Emery, P., Steer, S., and Hocking, L.J. (2010). Overlapping genetic susceptibility variants between three autoimmune disorders: Rheumatoid arthritis, type 1 diabetes and coeliac disease. Arthritis Res. Ther.","DOI":"10.1186\/ar3139"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2169","DOI":"10.1136\/ard.2009.126938","article-title":"Investigation of type 1 diabetes and coeliac disease susceptibility loci for association with juvenile idiopathic arthritis","volume":"69","author":"Hinks","year":"2010","journal-title":"Ann. Rheum. Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/j.immuni.2004.06.018","article-title":"A direct role for NKG2D\/MICA interaction in villous atrophy during celiac disease","volume":"21","author":"Hue","year":"2004","journal-title":"Immunity"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"228","DOI":"10.3109\/00365529509093269","article-title":"Confocal laser scanning microscopy of small-intestinal mucosa in celiac disease","volume":"30","author":"Magnusson","year":"1995","journal-title":"Scand. J. Gastroenterol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1006\/cbir.2002.0857","article-title":"Mechanical aspects of cell shape regulation and signaling","volume":"26","author":"Goldmann","year":"2002","journal-title":"Cell Biol. Int."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Bhattacharya, S., Nanayakkara, M., Kosova, R., Lania, G., Sarno, M., Gaito, A., Galatola, M., Greco, L., Cuomo, M., and Troncone, R. (2013). A celiac cellular phenotype, with altered LPP sub-cellular distribution, is inducible in controls by the toxic gliadin peptide p31\u201343. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0079763"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1763","DOI":"10.1074\/mcp.M800196-MCP200","article-title":"Investigation of protein-tyrosine phosphatase 1B function by quantitative proteomics","volume":"7","author":"Mertins","year":"2008","journal-title":"Mol. Cell. Proteom."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1834","DOI":"10.1073\/pnas.0304242101","article-title":"The role of protein tyrosine phosphatase 1B in ras signaling","volume":"101","author":"Dube","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Trackman, P.C., Nanayakkara, M., Lania, G., Maglio, M., Kosova, R., Sarno, M., Gaito, A., Discepolo, V., Troncone, R., and Auricchio, S. (2013). Enterocyte proliferation and signaling are constitutively altered in celiac disease. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0076006"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1016\/j.jss.2014.01.019","article-title":"T-cell activation Rho GTPase\u2013activating protein expression varies with inflammation location and severity in Crohn\u2019s disease","volume":"190","author":"Connelly","year":"2014","journal-title":"J. Surg. Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1145","DOI":"10.1097\/DCR.0b013e3182676931","article-title":"Mutation in tagap is protective of anal sepsis in ileocolic crohn\u2019s disease","volume":"55","author":"Connelly","year":"2012","journal-title":"Dis. Colon Rectum"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/S0962-8924(02)00004-1","article-title":"Rho GTPase-activating proteins in cell regulation","volume":"13","author":"Moon","year":"2003","journal-title":"Trends Cell Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1016\/S0968-0004(01)01973-9","article-title":"Dbl family guanine nucleotide exchange factors","volume":"26","author":"Zheng","year":"2001","journal-title":"Trends Biochem. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1016\/0168-9525(94)90114-7","article-title":"Gaps for rho-related GTPases","volume":"10","author":"Lamarche","year":"1994","journal-title":"Trends Genet."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"165","DOI":"10.2217\/fon.11.143","article-title":"Targeting rho GTPase signaling for cancer therapy","volume":"8","author":"Mardilovich","year":"2012","journal-title":"Future Oncol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1152\/physrev.00045.2010","article-title":"Inhibition and termination of physiological responses by GTPase activating proteins","volume":"92","author":"Ligeti","year":"2012","journal-title":"Physiol. Rev."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"4195","DOI":"10.1093\/hmg\/ddp365","article-title":"Common and different genetic background for rheumatoid arthritis and coeliac disease","volume":"18","author":"Coenen","year":"2009","journal-title":"Hum. Mol. Genet."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Sperandeo, M.P., Tosco, A., Izzo, V., Tucci, F., Troncone, R., Auricchio, R., Romanos, J., Trynka, G., Auricchio, S., and Jabri, B. (2011). Potential celiac patients: A model of celiac disease pathogenesis. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0021281"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1365","DOI":"10.1093\/aje\/kwr025","article-title":"Systematic review and meta-analysis of the association between complement component 3 and age-related macular degeneration: A huge review and meta-analysis","volume":"173","author":"Thakkinstian","year":"2011","journal-title":"Am. J. Epidemiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1136\/jmg.2008.061457","article-title":"Six new coeliac disease loci replicated in an italian population confirm association with coeliac disease","volume":"46","author":"Romanos","year":"2008","journal-title":"J. Med. Genet."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/j.tig.2004.06.014","article-title":"Meta-analysis of genetic association studies","volume":"20","author":"Flint","year":"2004","journal-title":"Trends Genet."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2157","DOI":"10.1074\/jbc.M206106200","article-title":"The focal adhesion and nuclear targeting capacity of the LIM-containing lipoma-preferred partner (LPP) protein","volume":"278","author":"Petit","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1161\/01.RES.0000261351.54147.de","article-title":"Angiotensin II, focal adhesion kinase, and PRX1 enhance smooth muscle expression of lipoma preferred partner and its newly identified binding partner palladin to promote cell migration","volume":"100","author":"Jin","year":"2007","journal-title":"Circ. Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1017\/S0029665109001074","article-title":"Session 3: Joint nutrition society and irish nutrition and dietetic institute symposium on \u201cnutrition and autoimmune disease\u201d","volume":"68","author":"Feighery","year":"2009","journal-title":"Proc. Nutr. Soc."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1007\/s00281-012-0312-1","article-title":"From genome-wide association studies to disease mechanisms: Celiac disease as a model for autoimmune diseases","volume":"34","author":"Kumar","year":"2012","journal-title":"Semin. Immunopathol."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/14\/2\/171\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T18:27:54Z","timestamp":1760207274000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/14\/2\/171"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,2,10]]},"references-count":38,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2017,2]]}},"alternative-id":["ijerph14020171"],"URL":"https:\/\/doi.org\/10.3390\/ijerph14020171","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,2,10]]}}}