Роль белка-организатора системы планарной клеточной полярности (CELSR1) в развитии первичной лимфедемы

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Роль белка-организатора системы планарной клеточной полярности (CELSR1) в развитии первичной лимфедемы. Флебология. 2024;(2):163-172

Лимфедема — заболевание, характеризующееся застоем богатой белком жидкости в интерстициальных тканях, когда скорость продукции лимфы превышает скорость ее удаления. Первичная лимфедема возникает вследствие врожденной дисплазии, гипоплазии или гиперплазии компонентов лимфатической системы, вызванной генетическими нарушениями, и в большинстве случаев связана с сигнальным путем рецептора фактора роста эндотелия сосудов 3 (Vascular Endothelial Growth Factor Receptor 3, VEGFR3), который отвечает за эмбриональный лимфангиогенез. Известно, что патогенные мутации в генах, вовлеченных в формирование морфологически правильной структуры сосудов, также могут быть связаны с развитием первичной лимфедемы. В обзоре рассмотрена роль CELSR1, белка-организатора системы планарной клеточной полярности, в развитии, функционировании и патологиях лимфатической системы.

Ключевые слова:

первичная лимфедема

CELSR1

полярность клеток

Авторы:

Филина Ю.В.

ФГАУОУ ВО «Казанский (Приволжский) федеральный университет»

ORCID: 0000-0002-7808-7279

Фейсханов А.К.

ФГАУОУ ВО «Казанский (Приволжский) федеральный университет»

ORCID: 0000-0002-9547-1395

Ибрагимова А.Р.

ФГБУН «Институт биоорганической химии им. академиков М.М. Шемякина и Ю.А. Овчинникова» Российской академии наук

ORCID: 0000-0001-7457-665X

Ризванов А.А.

ФГАУОУ ВО «Казанский (Приволжский) федеральный университет»

ORCID: 0000-0002-9427-5739

Мифтахова Р.Р.

ФГАУОУ ВО «Казанский (Приволжский) федеральный университет»

ORCID: 0000-0002-6686-1968

Дата поступления:

03.11.2023

Дата принятия в печать:

26.12.2023

Список литературы:

Maltese PE, Michelini S, Ricci M, et al. Increasing evidence of hereditary lymphedema caused by CELSR1 loss-of-function variants. Am J Med Genet A. Sep 2019;179(9):1718-1724. https://doi.org/10.1002/ajmg.a.61269
Rockson SG, Rivera KK. Estimating the population burden of lymphedema. Ann N Y Acad Sci. 2008;1131:147-154. https://doi.org/10.1196/annals.1413.014
Greene AK. Epidemiology and Morbidity of Lymphedema. In: Greene AK, Slavin SA, Brorson H, eds. Lymphedema: Presentation, Diagnosis, and Treatment. Springer International Publishing; 2015;33-44.
Brouillard P, Boon L, Vikkula M. Genetics of lymphatic anomalies. J Clin Invest. 2014;124(3):898-904. https://doi.org/10.1172/jci71614
Mendola A, Schlögel MJ, Ghalamkarpour A, Irrthum A, Nguyen HL, Fastré E, Bygum A, van der Vleuten C, Fagerberg C, Baselga E, Quere I, Mulliken JB, Boon LM, Brouillard P, Vikkula M; Lymphedema Research Group. Mutations in the VEGFR3 signaling pathway explain 36% of familial lymphedema. Mol Syndromol. 2013;4(6):257-266. https://doi.org/10.1159/000354097
Iljin K, Karkkainen MJ, Lawrence EC, Kimak MA, Uutela M, Taipale J, Pajusola K, Alhonen L, Halmekytö M, Finegold DN, Ferrell RE, Alitalo K. VEGFR3 gene structure, regulatory region, and sequence polymorphisms. The FASEB Journal. 2001;15(6):1028-1034. https://doi.org/10.1096/fsb2fj000383com
Brice G, Child AH, Evans A, Bell R, Mansour S, Burnand K, Sarfarazi M, Jeffery S, Mortimer P. Milroy disease and the <em>VEGFR-3</em> mutation phenotype. Journal of Medical Genetics. 2005;42(2):98-102. https://doi.org/10.1136/jmg.2004.024802
Dai T, Li B, He B, Yan L, Gu L, Liu X, Qi J, Li P, Zhou X. A novel mutation in the conserved sequence of vascular endothelial growth factor receptor 3 leads to primary lymphoedema. J Int Med Res. 2018;46(8):3162-3171. https://doi.org/10.1177/0300060518773264
Bonetti G, Paolacci S, Samaja M, Maltese PE, Michelini S, Michelini S, Michelini S, Ricci M, Cestari M, Dautaj A, Medori MC, Bertelli M. Low Efficacy of Genetic Tests for the Diagnosis of Primary Lymphedema Prompts Novel Insights into the Underlying Molecular Pathways. Int J Mol Sci. 2022;23(13) https://doi.org/10.3390/ijms23137414
Simons M, Mlodzik M. Planar cell polarity signaling: from fly development to human disease. Annu Rev Genet. 2008;42:517-540. https://doi.org/10.1146/annurev.genet.42.110807.091432
Hamann J, Aust G, Araç D, Engel FB, Formstone C, Fredriksson R, Hall RA, Harty BL, Kirchhoff C, Knapp B, Krishnan A, Liebscher I, Lin HH, Martinelli DC, Monk KR, Peeters MC, Piao X, Prömel S, Schöneberg T, Schwartz TW, Singer K, Stacey M, Ushkaryov YA, Vallon M, Wolfrum U, Wright MW, Xu L, Langenhan T, Schiöth HB. International Union of Basic and Clinical Pharmacology. XCIV. Adhesion G protein-coupled receptors. Pharmacol Rev. 2015;67(2):338-367. https://doi.org/10.1124/pr.114.009647
Formstone CJ. 7TM-Cadherins: developmental roles and future challenges. Adv Exp Med Biol. 2010;706:14-36. https://doi.org/10.1007/978-1-4419-7913-1_2
Chen WS, Antic D, Matis M, Logan CY, Povelones M, Anderson GA, Nusse R, Axelrod JD. Asymmetric homotypic interactions of the atypical cadherin flamingo mediate intercellular polarity signaling. Cell. 2008;133(6): 1093-1105. https://doi.org/10.1016/j.cell.2008.04.048
Joshi B, Gaur H, Hui SP, Patra C. Celsr family genes are dynamically expressed in embryonic and juvenile zebrafish. Dev Neurobiol. 2022;82(2): 192-213. https://doi.org/10.1002/dneu.22868
UniProt C. UniProt: the Universal Protein Knowledgebase in 2023. Nucleic Acids Res. 2023;51(D1):D523-D531. https://doi.org/10.1093/nar/gkac1052
Curtin JA, Quint E, Tsipouri V, Arkell RM, Cattanach B, Copp AJ, Henderson DJ, Spurr N, Stanier P, Fisher EM, Nolan PM, Steel KP, Brown SD, Gray IC, Murdoch JN. Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr Biol. 2003;13(13):1129-1133. https://doi.org/10.1016/s0960-9822(03)00374-9
Devenport D, Fuchs E. Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nat Cell Biol. 2008;10(11):1257-1268. https://doi.org/10.1038/ncb1784
Ravni A, Qu Y, Goffinet AM, Tissir F. Planar cell polarity cadherin Celsr1 regulates skin hair patterning in the mouse. J Invest Dermatol. 2009;129(10):2507-9. https://doi.org/10.1038/jid.2009.84
Formstone CJ, Moxon C, Murdoch J, Little P, Mason I. Basal enrichment within neuroepithelia suggests novel function(s) for Celsr1 protein. Mol Cell Neurosci. 2010;44(3):210-222. https://doi.org/10.1016/j.mcn.2010.03.008
Tatin F, Taddei A, Weston A, Fuchs E, Devenport D, Tissir F, Makinen T. Planar cell polarity protein Celsr1 regulates endothelial adherens junctions and directed cell rearrangements during valve morphogenesis. Dev Cell. 2013;26(1):31-44. https://doi.org/10.1016/j.devcel.2013.05.015
Ghimire SR, Ratzan EM, Deans MR. A non-autonomous function of the core PCP protein VANGL2 directs peripheral axon turning in the developing cochlea. Development. 2018;145(12). https://doi.org/10.1242/dev.159012
Simon F, Tissir F, Michel V, Lahlou G, Deans M, Beraneck M. Implication of Vestibular Hair Cell Loss of Planar Polarity for the Canal and Otolith-Dependent Vestibulo-Ocular Reflexes in Celsr1(–/–) Mice. Front Neurosci. 2021;15:750596. https://doi.org/10.3389/fnins.2021.750596
Stahley SN, Basta LP, Sharan R, Devenport D. Celsr1 adhesive interactions mediate the asymmetric organization of planar polarity complexes. Elife. 2021;10. https://doi.org/10.7554/eLife.62097
Usami FM, Arata M, Shi D, Oka S, Higuchi Y, Tissir F, Takeichi M, Fujimori T. Intercellular and intracellular cilia orientation is coordinated by CELSR1 and CAMSAP3 in oviduct multi-ciliated cells. J Cell Sci. 2021;134(4):jcs257006. https://doi.org/10.1242/jcs.257006
Krishnan A, Samtani R, Dhanantwari P, Lee E, Yamada S, Shiota K, Donofrio MT, Leatherbury L, Lo CW. A detailed comparison of mouse and human cardiac development. Pediatr Res. 2014;76(6):500-507. https://doi.org/10.1038/pr.2014.128
Alitalo K. The lymphatic vasculature in disease. Nat Med. 2011;17(11): 1371-1380. https://doi.org/10.1038/nm.2545
Gonzalez-Garay ML, Aldrich MB, Rasmussen JC, Guilliod R, Lapinski PE, King PD, Sevick-Muraca EM. A novel mutation in CELSR1 is associated with hereditary lymphedema. Vasc Cell. 2016;8:1. https://doi.org/10.1186/s13221-016-0035-5
Erickson RP, Lai LW, Mustacich DJ, Bernas MJ, Kuo PH, Witte MH. Sex-limited penetrance of lymphedema to females with CELSR1 haploinsufficiency: A second family. Clin Genet. 2019;96(5):478-482. https://doi.org/10.1111/cge.13622
Seo SH, Lee S, Park JK, Yang EJ, Kim B, Lee JS, Kim MJ, Park SS, Seong MW, Nam SY, Heo CY, Myung Y. Clinical staging and genetic profiling of Korean patients with primary lymphedema using targeted gene sequencing. Sci Rep. 2022;12(1):13591. https://doi.org/10.1038/s41598-022-17958-7
Sudduth CL, Smits PJ, Cheng YS, Schmitz-Abe K, Agrawal P, Greene AK. Primary Upper Extremity Lymphedema Caused by a CELSR1 Variant. Journal of Vascular Anomalies. 2022;3(2):e041. https://doi.org/10.1097/jova.0000000000000041
Goss JA, Maclellan RA, Greene AK. Primary Lymphedema of the Upper Extremities: Clinical and Lymphoscintigraphic Features in 23 Patients. Lymphat Res Biol. 2019;17(1):40-44. https://doi.org/10.1089/lrb.2017.0085
Palumbo P, Accadia M, Leone MP, Palladino T, Stallone R, Carella M, Palumbo O. Clinical and molecular characterization of an emerging chromosome 22q13.31 microdeletion syndrome. Am J Med Genet A. 2018;176(2): 391-398. https://doi.org/10.1002/ajmg.a.38559
Xia S, Liu Z, Yan H, Chang K, Sun Y, Wang J, Shen W. Lymphedema complicated by protein-losing enteropathy with a 22q13.3 deletion and the potential role of CELSR1: A case report. Medicine (Baltimore). 2021;100(24):e26307. https://doi.org/10.1097/MD.0000000000026307
McCoy MD, Sarasua SM, DeLuca JM, Davis S, Phelan K, Rogers RC, Boccuto L. State of the Science for Kidney Disorders in Phelan-McDermid Syndrome: UPK3A, FBLN1, WNT7B, and CELSR1 as Candidate Genes. Genes (Basel). 2022;13(6):1042. https://doi.org/10.3390/genes13061042
Juriloff DM, Harris MJ. A consideration of the evidence that genetic defects in planar cell polarity contribute to the etiology of human neural tube defects. Birth Defects Res A Clin Mol Teratol. 2012;94(10):824-840. https://doi.org/10.1002/bdra.23079
Robinson A, Escuin S, Doudney K, Vekemans M, Stevenson RE, Greene ND, Copp AJ, Stanier P. Mutations in the planar cell polarity genes CELSR1 and SCRIB are associated with the severe neural tube defect craniorachischisis. Hum Mutat. 2012;33(2):440-447. https://doi.org/10.1002/humu.21662
Lei Y, Zhu H, Yang W, Ross ME, Shaw GM, Finnell RH. Identification of novel CELSR1 mutations in spina bifida. PLoS One. 2014;9(3):e92207. https://doi.org/10.1371/journal.pone.0092207
Wang L, Xiao Y, Tian T, Jin L, Lei Y, Finnell RH, Ren A. Digenic variants of planar cell polarity genes in human neural tube defect patients. Digenic variants of planar cell polarity genes in human neural tube defect patients. Mol Genet Metab. 2018;124(1):94-100. https://doi.org/10.1016/j.ymgme.2018.03.005
Munteanu O, Cîrstoiu MM, Filipoiu FM, Neamţu MN, Stavarache I, Georgescu TA, Bratu OG, Iorgulescu G, Bohîlţea RE. The etiopathogenic and morphological spectrum of anencephaly: a comprehensive review of literature. Rom J Morphol Embryol. 2020;61(2):335-343. https://doi.org/10.47162/RJME.61.2.03
Tian T, Lei Y, Chen Y, Karki M, Jin L, Finnell RH, Wang L, Ren A. Somatic mutations in planar cell polarity genes in neural tissue from human fetuses with neural tube defects. Hum Genet. 2020;139(10):1299-1314. https://doi.org/10.1007/s00439-020-02172-0
Florio M, Huttner WB. Neural progenitors, neurogenesis and the evolution of the neocortex. Development. 2014;141(11):2182-2194. https://doi.org/10.1242/dev.090571
Rommelse NN, Franke B, Geurts HM, Hartman CA, Buitelaar JK. Shared heritability of attention-deficit/hyperactivity disorder and autism spectrum disorder. Eur Child Adolesc Psychiatry. 2010;19(3):281-295. https://doi.org/10.1007/s00787-010-0092-x
Wegiel J, Kuchna I, Nowicki K, Imaki H, Wegiel J, Marchi E, Ma SY, Chauhan A, Chauhan V, Bobrowicz TW, de Leon M, Louis LA, Cohen IL, London E, Brown WT, Wisniewski T. The neuropathology of autism: defects of neurogenesis and neuronal migration, and dysplastic changes. Acta Neuropathol. 2010;119(6):755-770. https://doi.org/10.1007/s00401-010-0655-4
Salasova A, Yokota C, Potesil D, Zdrahal Z, Bryja V, Arenas E. A proteomic analysis of LRRK2 binding partners reveals interactions with multiple signaling components of the WNT/PCP pathway. Mol Neurodegener. 2017;12(1):54. https://doi.org/10.1186/s13024-017-0193-9
Yemni EA, Monies D, Alkhairallah T, et al. Integrated Analysis of Whole Exome Sequencing and Copy Number Evaluation in Parkinson’s Disease. Sci Rep. 2019;9(1):3344. https://doi.org/10.1038/s41598-019-40102-x
Tham YC, Li X, Wong TY, Quigley HA, Aung T, Cheng CY. Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology. 2014;121(11):2081-2090. https://doi.org/10.1016/j.ophtha.2014.05.013
Zhao M, Ma P, Xie Q, Bui AD, Yonamine S, Hinterwirth A, Zhong L, Chen C, Doan T, Han Y. Biomarkers for primary open-angle glaucoma progression. Exp Eye Res. 2022;219:109025. https://doi.org/10.1016/j.exer.2022.109025
Gross J, Grimm O, Ortega G, Teuber I, Lesch KP, Meyer J. Mutational analysis of the neuronal cadherin gene CELSR1 and exclusion as a candidate for catatonic schizophrenia in a large family. Psychiatr Genet. 2001;11(4): 197-200. https://doi.org/10.1097/00041444-200112000-00003
Kuure S, Cebrian C, Machingo Q, Lu BC, Chi X, Hyink D, D’Agati V, Gurniak C, Witke W, Costantini F. Actin depolymerizing factors cofilin1 and destrin are required for ureteric bud branching morphogenesis. PLoS Genet. 2010;6(10):e1001176. https://doi.org/10.1371/journal.pgen.1001176
Packard A, Georgas K, Michos O, Riccio P, Cebrian C, Combes AN, Ju A, Ferrer-Vaquer A, Hadjantonakis AK, Zong H, Little MH, Costantini F. Luminal mitosis drives epithelial cell dispersal within the branching ureteric bud. Dev Cell. 2013;27(3):319-330. https://doi.org/10.1016/j.devcel.2013.09.001
Brzóska HŁ, d’Esposito AM, Kolatsi-Joannou M, Patel V, Igarashi P, Lei Y, Finnell RH, Lythgoe MF, Woolf AS, Papakrivopoulou E, Long DA. Planar cell polarity genes Celsr1 and Vangl2 are necessary for kidney growth, differentiation, and rostrocaudal patterning. Kidney Int. 2016;90(6):1274-1284. https://doi.org/10.1016/j.kint.2016.07.011
Schnell U, Carroll TJ. Planar cell polarity of the kidney. Exp Cell Res. 2016; 343(2):258-266. https://doi.org/10.1016/j.yexcr.2014.11.003
Skalická K, Hrčková G, Vaská A, Baranyaiová A, Janega P, Žilinská Z, Daniš D, Kovács L. Pilot Study of the Occurrence of Somatic Mutations in Ciliary Signalling Pathways as a Contribution Factor to Autosomal Dominant Polycystic Kidney Development. Folia Biol (Praha). 2017;63(5-6):174-181.
Ueyama C, Horibe H, Fujimaki T, Oguri M, Kato K, Yamada Y. Association of genetic variants of CELSR1 and 3q28 with hypertension in community-dwelling individuals. Biomed Rep. 2013;1(6):840-844. https://doi.org/10.3892/br.2013.168
Shi D, Komatsu K, Hirao M, Toyooka Y, Koyama H, Tissir F, Goffinet AM, Uemura T, Fujimori T. Celsr1 is required for the generation of polarity at multiple levels of the mouse oviduct. Development. 2014;141(23):4558-4568. https://doi.org/10.1242/dev.115659
Zhang S, Cheng J, Quan C, Wen H, Feng Z, Hu Q, Zhu J, Huang Y, Wu X. circCELSR1 (hsa_circ_0063809) Contributes to Paclitaxel Resistance of Ovarian Cancer Cells by Regulating FOXR2 Expression via miR-1252. Mol Ther Nucleic Acids. 2020;19:718-730. https://doi.org/10.1016/j.omtn.2019.12.005
Wei S, Qi L, Wang L. Overexpression of circ_CELSR1 facilitates paclitaxel resistance of ovarian cancer by regulating miR-149-5p/SIK2 axis. Anticancer Drugs. 2021;32(5):496-507. https://doi.org/10.1097/CAD.0000000000001058
Ghafouri-Fard S, Khoshbakht T, Hussen BM, Taheri M, Samsami M. Emerging role of circular RNAs in the pathogenesis of ovarian cancer. Cancer Cell Int. 2022;22(1):172. https://doi.org/10.1186/s12935-022-02602-1
Wang C, Xue W, Zhang H, Fu Y. Identification of candidate genes encoding tumor-specific neoantigens in early- and late-stage colon adenocarcinoma. Aging (Albany NY). 2021;13(3):4024-4044. https://doi.org/10.18632/aging.202370
Xie F, Gleue CA, Deschaine M, Dasari S, Lau JS, Sartori-Valinotti JC, Meves A, Lehman JS. Whole-exome sequencing of transforming oral lichen planus reveals mutations in DNA damage repair and apoptosis pathway genes. J Oral Pathol Med. 2022;51(4):395-404. https://doi.org/10.1111/jop.13284
Wang G, Li Y, Zhang D, Zhao S, Zhang Q, Luo C, Sun X, Zhang B. CELSR1 Acts as an Oncogene Regulated by miR-199a-5p in Glioma. Cancer Manag Res. 2020;12:8857-8865. https://doi.org/10.2147/CMAR.S258835
Wang J, Sun C, Liu M, Zang D, Wang C, Liu Q, Liu Y, Chen Q. The potentially therapeutic targets of pediatric anaplastic ependymoma by transcriptome profiling. Neoplasma. 2021;68(1):53-61. https://doi.org/10.4149/neo_2020_200529N581
Terkelsen T, Pernemalm M, Gromov P, Børresen-Dale AL, Krogh A, Haakensen VD, Lethiö J, Papaleo E, Gromova I. High-throughput proteomics of breast cancer interstitial fluid: identification of tumor subtype-specific serologically relevant biomarkers. Mol Oncol. 2021;15(2):429-461. https://doi.org/10.1002/1878-0261.12850
Geradts J, Groth J, Wu Y, Jin G. Validation of an oligo-gene signature for the prognostic stratification of ductal carcinoma in situ (DCIS). Breast Cancer Res Treat. 2016;157(3):447-459. https://doi.org/10.1007/s10549-016-3838-4
Li Y, Zhang H, Fan L, Mou J, Yin Y, Peng C, Chen Y, Lu H, Zhao L, Tao Z, Chen J, Wang Y, Qi X, Huang R, Ren J. MiR-629-5p promotes the invasion of lung adenocarcinoma via increasing both tumor cell invasion and endothelial cell permeability. Oncogene. 2020;39(17):3473-3488. https://doi.org/10.1038/s41388-020-1228-1
Zeng XY, Yuan J, Wang C, Zeng D, Yong JH, Jiang XY, Lan H, Xiao SS. circCELSR1 facilitates ovarian cancer proliferation and metastasis by sponging miR-598 to activate BRD4 signals. Mol Med. 2020;26(1):70. https://doi.org/10.1186/s10020-020-00194-y
Theis JL, Niaz T, Sundsbak RS, Fogarty ZC, Bamlet WR, Hagler DJ, Olson TM. CELSR1 Risk Alleles in Familial Bicuspid Aortic Valve and Hypoplastic Left Heart Syndrome. Circ Genom Precis Med. 2022;15(2):e003523. https://doi.org/10.1161/CIRCGEN.121.003523
Qiao X, Liu Y, Li P, Chen Z, Li H, Yang X, Finnell RH, Yang Z, Zhang T, Qiao B, Zheng Y, Wang H. Genetic analysis of rare coding mutations of CELSR1-3 in congenital heart and neural tube defects in Chinese people. Clin Sci (Lond). 2016;130(24):2329-2340. https://doi.org/10.1042/CS20160686
Yamada Y, Fuku N, Tanaka M, Aoyagi Y, Sawabe M, Metoki N, Yoshida H, Satoh K, Kato K, Watanabe S, Nozawa Y, Hasegawa A, Kojima T. Identification of CELSR1 as a susceptibility gene for ischemic stroke in Japanese individuals by a genome-wide association study. Atherosclerosis. 2009;207(1): 144-149. https://doi.org/10.1016/j.atherosclerosis.2009.03.038
Gouveia LO, Sobral J, Vicente AM, Ferro JM, Oliveira SA. Replication of the CELSR1 association with ischemic stroke in a Portuguese case-control cohort. Atherosclerosis. 2011;217(1):260-262. https://doi.org/10.1016/j.atherosclerosis.2011.03.022
Zhan YH, Lin Y, Tong SJ, Ma QL, Lu CX, Fang L, Wei W, Cai B, Wang N. The CELSR1 polymorphisms rs6007897 and rs4044210 are associated with ischaemic stroke in Chinese Han population. Ann Hum Biol. 2015;42(1):26-30. https://doi.org/10.3109/03014460.2014.944214
Wang LH, Zhang GL, Liu XY, Peng A, Ren HY, Huang SH, Liu T, Wang XJ. CELSR1 Promotes Neuroprotection in Cerebral Ischemic Injury Mainly Through the Wnt/PKC Signaling Pathway. Int J Mol Sci. 2020;21(4):1267. https://doi.org/10.3390/ijms21041267
Hardin M, Cho MH, Sharma S, Glass K, Castaldi PJ, McDonald ML, Aschard H, Senter-Sylvia J, Tantisira K, Weiss ST, Hersh CP, Morrow JD, Lomas D, Agusti A, Bakke P, Gulsvik A, O’Connor GT, Dupuis J, Hokanson J, Crapo JD, Beaty TH, Laird N, Silverman EK, DeMeo DL; COPDGene and Evaluation of COPD Longitudinally to Identify Predictive Surrogate End-Points Investigators. Sex-Based Genetic Association Study Identifies CELSR1 as a Possible Chronic Obstructive Pulmonary Disease Risk Locus among Women. Am J Respir Cell Mol Biol. 2017;56(3):332-341. https://doi.org/10.1165/rcmb.2016-0172OC
Tseng CC, Lin YZ, Lin CH, Li RN, Yen CY, Chan HC, Tsai WC, Ou TT, Wu CC, Sung WY, Yen JH. Next-Generation Sequencing Profiles of the Methylome and Transcriptome in Peripheral Blood Mononuclear Cells of Rheumatoid Arthritis. J Clin Med. 2019;8(9):1284. https://doi.org/10.3390/jcm8091284
An JY, Jung JH, Choi L, Wieben ED, Mohney BG. Identification of Possible Risk Variants of Familial Strabismus Using Exome Sequencing Analysis. Genes (Basel). 2021;12(1):75. https://doi.org/10.3390/genes12010075
Klinner J, Krüger M, Brunet T, Makowski C, Riedhammer KM, Mollweide A, Wagner M, Hoefele J. Congenital lymphedema as a rare and first symptom of tuberous sclerosis complex. Gene. 2020;753:144815. https://doi.org/10.1016/j.gene.2020.144815
Gordon K, Mortimer PS, van Zanten M, Jeffery S, Ostergaard P, Mansour S. The St George’s Classification Algorithm of Primary Lymphatic Anomalies. Lymphat Res Biol. 2021;19(1):25-30. https://doi.org/10.1089/lrb.2020.0104

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