User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Pathogenetics of alveolar capillary dysplasia with misalignment of pulmonary veins.

Primary tabs

Szafranski, Przemyslaw Gambin, Tomasz Dharmadhikari, Avinash V Akdemir, Kadir Caner Jhangiani, Shalini N Sznajer, Yves [UCL] Stankiewicz, Paweł

Alveolar capillary dysplasia with misalignment of pulmonary veins (ACDMPV) is a lethal lung developmental disorder caused by heterozygous point mutations or genomic deletion copy-number variants (CNVs) of FOXF1 or its upstream enhancer involving fetal lung-expressed long noncoding RNA genes LINC01081 and LINC01082. Using custom-designed array comparative genomic hybridization, Sanger sequencing, whole exome sequencing (WES), and bioinformatic analyses, we studied 22 new unrelated families (20 postnatal and two prenatal) with clinically diagnosed ACDMPV. We describe novel deletion CNVs at the FOXF1 locus in 13 unrelated ACDMPV patients. Together with the previously reported cases, all 31 genomic deletions in 16q24.1, pathogenic for ACDMPV, for which parental origin was determined, arose de novo with 30 of them occurring on the maternally inherited chromosome 16, strongly implicating genomic imprinting of the FOXF1 locus in human lungs. Surprisingly, we have also identified four ACDMPV families with the pathogenic variants in the FOXF1 locus that arose on paternal chromosome 16. Interestingly, a combination of the severe cardiac defects, including hypoplastic left heart, and single umbilical artery were observed only in children with deletion CNVs involving FOXF1 and its upstream enhancer. Our data demonstrate that genomic imprinting at 16q24.1 plays an important role in variable ACDMPV manifestation likely through long-range regulation of FOXF1 expression, and may be also responsible for key phenotypic features of maternal uniparental disomy 16. Moreover, in one family, WES revealed a de novo missense variant in ESRP1, potentially implicating FGF signaling in the etiology of ACDMPV.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2016
Language Anglais
Journal information "Human Genetics" - Vol. 135, no.5, p. 569-586 (2016)
Peer reviewed yes
Publisher Springer Verlag ((Germany) Berlin )
issn 0340-6717
e-issn 1432-1203
Publication status Publié
Affiliations UCL - SSS/IREC/SLUC - Pôle St.-Luc
UCL - (SLuc) Centre de génétique médicale UCL
MESH Subject Chromosomes, Human, Pair 16 ; Infant, Newborn ; Male ; Pedigree ; Persistent Fetal Circulation Syndrome ; Pulmonary Alveoli ; Pulmonary Veins ; Sequence Deletion ; Comparative Genomic Hybridization ; Female ; Forkhead Transcription Factors ; Genes, Lethal ; Genome, Human ; Genomic Imprinting ; High-Throughput Nucleotide Sequencing ; Humans
Links
  1. Araujo Júnior E., Palma-Dias R., Martins W. P., Reidy K., da Silva Costa F., Congenital heart disease and adverse perinatal outcome in fetuses with confirmed isolated single functioning umbilical artery, 10.3109/01443615.2014.935720
  2. Barlow D. P., Bartolomei M. S., Genomic Imprinting in Mammals, 10.1101/cshperspect.a018382
  3. Bartolomei M. S., Ferguson-Smith A. C., Mammalian Genomic Imprinting, 10.1101/cshperspect.a002592
  4. Bishop Naomi B., Stankiewicz Pawel, Steinhorn Robin H., Alveolar Capillary Dysplasia, 10.1164/rccm.201010-1697ci
  5. Black Brian L., Olson Eric N., TRANSCRIPTIONAL CONTROL OF MUSCLE DEVELOPMENT BY MYOCYTE ENHANCER FACTOR-2 (MEF2) PROTEINS, 10.1146/annurev.cellbio.14.1.167
  6. Brand Nigel J., Myocyte enhancer factor 2 (MEF2), 10.1016/s1357-2725(97)00084-8
  7. Campbell Ian M., Yuan Bo, Robberecht Caroline, Pfundt Rolph, Szafranski Przemyslaw, McEntagart Meriel E., Nagamani Sandesh C.S., Erez Ayelet, Bartnik Magdalena, Wiśniowiecka-Kowalnik Barbara, Plunkett Katie S., Pursley Amber N., Kang Sung-Hae L., Bi Weimin, Lalani Seema R., Bacino Carlos A., Vast Mala, Marks Karen, Patton Michael, Olofsson Peter, Patel Ankita, Veltman Joris A., Cheung Sau Wai, Shaw Chad A., Vissers Lisenka E.L.M., Vermeesch Joris R., Lupski James R., Stankiewicz Paweł, Parental Somatic Mosaicism Is Underrecognized and Influences Recurrence Risk of Genomic Disorders, 10.1016/j.ajhg.2014.07.003
  8. Campbell Ian M., Shaw Chad A., Stankiewicz Pawel, Lupski James R., Somatic mosaicism: implications for disease and transmission genetics, 10.1016/j.tig.2015.03.013
  9. Chang Vincent Wen-Hsing, Ho Ye-Shih, Structural characterization of the mouse Foxf1a gene, 10.1016/s0378-1119(01)00400-0
  10. Chu Dong, Kakazu Naoki, Gorrin-Rivas Manuel J., Lu Hai-Ping, Kawata Mitsuhiro, Abe Tatsuo, Ueda Kunihiro, Adachi Yoshifumi, Cloning and Characterization of LUN, a Novel RING Finger Protein That Is Highly Expressed in Lung and Specifically Binds to a Palindromic Sequence, 10.1074/jbc.m010262200
  11. Dello Russo Patrizia, Franzoni Alessandra, Baldan Federica, Puppin Cinzia, De Maglio Giovanna, Pittini Carla, Cattarossi Luigi, Pizzolitto Stefano, Damante Giuseppe, A 16q deletion involving FOXF1 enhancer is associated to pulmonary capillary hemangiomatosis, 10.1186/s12881-015-0241-7
  12. Dharmadhikari Avinash V., Szafranski Przemyslaw, V. Kalinichenko Vladimir, Stankiewicz Pawel, Genomic and Epigenetic Complexity of the FOXF1 Locus in 16q24.1: Implications for Development and Disease, 10.2174/1389202916666150122223252
  13. Dixon Jesse R., Selvaraj Siddarth, Yue Feng, Kim Audrey, Li Yan, Shen Yin, Hu Ming, Liu Jun S., Ren Bing, Topological domains in mammalian genomes identified by analysis of chromatin interactions, 10.1038/nature11082
  14. Fatica Alessandro, Bozzoni Irene, Long non-coding RNAs: new players in cell differentiation and development, 10.1038/nrg3606
  15. Ferguson-Smith Anne C., Genomic imprinting: the emergence of an epigenetic paradigm, 10.1038/nrg3032
  16. Galambos Csaba, Sims-Lucas Sunder, Ali Noorjahan, Gien Jason, Dishop Megan K, Abman Steven H, Intrapulmonary vascular shunt pathways in alveolar capillary dysplasia with misalignment of pulmonary veins, 10.1136/thoraxjnl-2014-205851
  17. Garabedian MJ, Wallerstein D, Medina N, Byrne J, Wallerstein RJ (2012) Prenatal diagnosis of cystic hygroma related to a deletion of 16q24.1 with haploinsufficiency of FOXF1 and FOXC2 genes. Case Rep Genet 2012:490408
  18. Gregg Christopher, Known unknowns for allele-specific expression and genomic imprinting effects, 10.12703/p6-75
  19. Grote Phillip, Wittler Lars, Hendrix David, Koch Frederic, Währisch Sandra, Beisaw Arica, Macura Karol, Bläss Gaby, Kellis Manolis, Werber Martin, Herrmann Bernhard G., The Tissue-Specific lncRNA Fendrr Is an Essential Regulator of Heart and Body Wall Development in the Mouse, 10.1016/j.devcel.2012.12.012
  20. Gu Shen, Yuan Bo, Campbell Ian M., Beck Christine R., Carvalho Claudia M.B., Nagamani Sandesh C.S., Erez Ayelet, Patel Ankita, Bacino Carlos A., Shaw Chad A., Stankiewicz Paweł, Cheung Sau Wai, Bi Weimin, Lupski James R., Alu-mediated diverse and complex pathogenic copy-number variants within human chromosome 17 at p13.3, 10.1093/hmg/ddv146
  21. Guo Ya, Xu Quan, Canzio Daniele, Shou Jia, Li Jinhuan, Gorkin David U., Jung Inkyung, Wu Haiyang, Zhai Yanan, Tang Yuanxiao, Lu Yichao, Wu Yonghu, Jia Zhilian, Li Wei, Zhang Michael Q., Ren Bing, Krainer Adrian R., Maniatis Tom, Wu Qiang, CRISPR Inversion of CTCF Sites Alters Genome Topology and Enhancer/Promoter Function, 10.1016/j.cell.2015.07.038
  22. Hamvas Aaron, Nogee Lawrence M., Wegner Daniel J., DePass Kelcey, Christodoulou John, Bennetts Bruce, McQuade Leon R., Gray Peter H., Deterding Robin R., Carroll Travis R., Kammesheidt Anja, Kasch Laura M., Kulkarni Shashikant, Cole F. Sessions, Inherited Surfactant Deficiency Caused by Uniparental Disomy of Rare Mutations in the Surfactant Protein-B and ATP Binding Cassette, Subfamily A, Member 3 Genes, 10.1016/j.jpeds.2009.06.006
  23. Handrigan Gregory Ryan, Chitayat David, Lionel Anath C, Pinsk Maury, Vaags Andrea K, Marshall Christian R, Dyack Sarah, Escobar Luis F, Fernandez Bridget A, Stegman Joseph C, Rosenfeld Jill A, Shaffer Lisa G, Goodenberger McKinsey, Hodge Jennelle C, Cain Jason E, Babul-Hirji Riyana, Stavropoulos Dimitri J, Yiu Verna, Scherer Stephen W, Rosenblum Norman D, Deletions in 16q24.2 are associated with autism spectrum disorder, intellectual disability and congenital renal malformation, 10.1136/jmedgenet-2012-101288
  24. Hastings P. J., Lupski James R., Rosenberg Susan M., Ira Grzegorz, Mechanisms of change in gene copy number, 10.1038/nrg2593
  25. Iascone M, Ciccone R, Galletti L, Marchetti D, Seddio F, Lincesso AR, Pezzoli L, Vetro A, Barachetti D, Boni L, Federici D, Soto AM, Comas JV, Ferrazzi P, Zuffardi O, Identification of de novo mutations and rare variants in hypoplastic left heart syndrome, 10.1111/j.1399-0004.2011.01674.x
  26. Jacques Pierre-Étienne, Jeyakani Justin, Bourque Guillaume, The Majority of Primate-Specific Regulatory Sequences Are Derived from Transposable Elements, 10.1371/journal.pgen.1003504
  27. Joza Stephen, Wang Jinxia, Fox Emily, Hillman Valerie, Ackerley Cameron, Post Martin, Loss of Semaphorin-Neuropilin-1 Signaling Causes Dysmorphic Vascularization Reminiscent of Alveolar Capillary Dysplasia, 10.1016/j.ajpath.2012.08.037
  28. Kagoshima Masako, Ito Takaaki, , Diverse gene expression and function of semaphorins in developing lung: positive and negative regulatory roles of semaphorins in lung branching morphogenesis, 10.1046/j.1365-2443.2001.00441.x
  29. Kalinichenko VV, Lim L, Shin B, Costa RH (2001) Differential expression of forkhead box transcription factors following butylated hydroxytoluene lung injury. Am J Physiol Lung Cell Mol Physiol 280:L695–L704
  30. Kim Il-Man, Zhou Yan, Ramakrishna Sneha, Hughes Douglas E., Solway Julian, Costa Robert H., Kalinichenko Vladimir V., Functional Characterization of Evolutionarily Conserved DNA Regions in Forkhead Box F1 Gene Locus, 10.1074/jbc.m506531200
  31. Kohlhase J�rgen, Janssen Bart, Weidenauer Karin, Harms Karsten, Bartels Iris, First confirmed case with paternal uniparental disomy of chromosome 16, 10.1002/(sici)1096-8628(20000320)91:3<190::aid-ajmg6>3.0.co;2-i
  32. Lai Ka-Man Venus, Gong Guochun, Atanasio Amanda, Rojas José, Quispe Joseph, Posca Julita, White Derek, Huang Mei, Fedorova Daria, Grant Craig, Miloscio Lawrence, Droguett Gustavo, Poueymirou William T., Auerbach Wojtek, Yancopoulos George D., Frendewey David, Rinn John, Valenzuela David M., Diverse Phenotypes and Specific Transcription Patterns in Twenty Mouse Lines with Ablated LincRNAs, 10.1371/journal.pone.0125522
  33. Langston Claire, Case 2 Misalignment of Pulmonary Veins and Alveolar Capillary Dysplasia, 10.3109/15513819109064753
  34. Luedi P. P., Dietrich F. S., Weidman J. R., Bosko J. M., Jirtle R. L., Hartemink A. J., Computational and experimental identification of novel human imprinted genes, 10.1101/gr.6584707
  35. Lupiáñez Darío G., Kraft Katerina, Heinrich Verena, Krawitz Peter, Brancati Francesco, Klopocki Eva, Horn Denise, Kayserili Hülya, Opitz John M., Laxova Renata, Santos-Simarro Fernando, Gilbert-Dussardier Brigitte, Wittler Lars, Borschiwer Marina, Haas Stefan A., Osterwalder Marco, Franke Martin, Timmermann Bernd, Hecht Jochen, Spielmann Malte, Visel Axel, Mundlos Stefan, Disruptions of Topological Chromatin Domains Cause Pathogenic Rewiring of Gene-Enhancer Interactions, 10.1016/j.cell.2015.04.004
  36. Mahlapuu M, Enerback S, Carlsson P (2001) Haploinsufficiency of the forkhead gene Foxf1, a target for sonic hedgehog signalling, causes lung and foregut malformations. Development 128:2397–2406
  37. Oyanagi Hiroki, Takenaka Kazumasa, Ishikawa Shinya, Kawano Yozo, Adachi Yoshifumi, Ueda Kunihiro, Wada Hiromi, Tanaka Fumihiro, Expression of LUN gene that encodes a novel RING finger protein is correlated with development and progression of non-small cell lung cancer, 10.1016/j.lungcan.2004.03.009
  38. Parris Toshima, Nik Ali Moussavi, Kotecha Sailesh, Langston Claire, Helou Khalil, Platt Craig, Carlsson Peter, Inversion upstream ofFOXF1in a case of lethal alveolar capillary dysplasia with misalignment of pulmonary veins, 10.1002/ajmg.a.35832
  39. Prothro Stephanie L., Plosa Erin, Markham Melinda, Szafranski Przemyslaw, Stankiewicz Pawel, Killen Stacy A.S., Prenatal Diagnosis of Alveolar Capillary Dysplasia with Misalignment of Pulmonary Veins, 10.1016/j.jpeds.2015.11.041
  40. Sauvageau Martin, Goff Loyal A, Lodato Simona, Bonev Boyan, Groff Abigail F, Gerhardinger Chiara, Sanchez-Gomez Diana B, Hacisuleyman Ezgi, Li Eric, Spence Matthew, Liapis Stephen C, Mallard William, Morse Michael, Swerdel Mavis R, D’Ecclessis Michael F, Moore Jennifer C, Lai Venus, Gong Guochun, Yancopoulos George D, Frendewey David, Kellis Manolis, Hart Ronald P, Valenzuela David M, Arlotta Paola, Rinn John L, Multiple knockout mouse models reveal lincRNAs are required for life and brain development, 10.7554/elife.01749
  41. Sen Partha, Thakur Nivedita, Stockton David W., Langston Claire, Bejjani Bassem A., Expanding the phenotype of alveolar capillary dysplasia (ACD), 10.1016/j.jpeds.2004.06.081
  42. Sen Partha, Gerychova Romana, Janku Petr, Jezova Marta, Valaskova Iveta, Navarro Colby, Silva Iris, Langston Claire, Welty Stephen, Belmont John, Stankiewicz Pawel, A familial case of alveolar capillary dysplasia with misalignment of pulmonary veins supports paternal imprinting of FOXF1 in human, 10.1038/ejhg.2012.171
  43. Sen Partha, Yang Yaping, Navarro Colby, Silva Iris, Szafranski Przemyslaw, Kolodziejska Katarzyna E., Dharmadhikari Avinash V., Mostafa Hasnaa, Kozakewich Harry, Kearney Debra, Cahill John B., Whitt Merrissa, Bilic Masha, Margraf Linda, Charles Adrian, Goldblatt Jack, Gibson Kathleen, Lantz Patrick E., Garvin A. Julian, Petty John, Kiblawi Zeina, Zuppan Craig, McConkie-Rosell Allyn, McDonald Marie T., Peterson-Carmichael Stacey L., Gaede Jane T., Shivanna Binoy, Schady Deborah, Friedlich Philippe S., Hays Stephen R., Palafoll Irene Valenzuela, Siebers-Renelt Ulrike, Bohring Axel, Finn Laura S., Siebert Joseph R., Galambos Csaba, Nguyen Lananh, Riley Melissa, Chassaing Nicolas, Vigouroux Adeline, Rocha Gustavo, Fernandes Susana, Brumbaugh Jane, Roberts Kari, Ho-ming Luk, Lo Ivan F. M., Lam Stephen, Gerychova Romana, Jezova Marta, Valaskova Iveta, Fellmann Florence, Afshar Katayoun, Giannoni Eric, Muhlethaler Vincent, Liang Jinlong, Beckmann Jacques S., Lioy Janet, Deshmukh Hitesh, Srinivasan Lakshmi, Swarr Daniel T., Sloman Melissa, Shaw-Smith Charles, van Loon Rosa Laura, Hagman Cecilia, Sznajer Yves, Barrea Catherine, Galant Christine, Detaille Thierry, Wambach Jennifer A., Cole F. Sessions, Hamvas Aaron, Prince Lawrence S., Diderich Karin E.M., Brooks Alice S., Verdijk Robert M., Ravindranathan Hari, Sugo Ella, Mowat David, Baker Michael L., Langston Claire, Welty Stephen, Stankiewicz Pawel, NovelFOXF1Mutations in Sporadic and Familial Cases of Alveolar Capillary Dysplasia with Misaligned Pulmonary Veins Imply a Role for its DNA Binding Domain, 10.1002/humu.22313
  44. Sen Partha, Dharmadhikari Avinash V., Majewski Tadeusz, Mohammad Mahmoud A., Kalin Tanya V., Zabielska Joanna, Ren Xiaomeng, Bray Molly, Brown Hannah M., Welty Stephen, Thevananther Sundararajah, Langston Claire, Szafranski Przemyslaw, Justice Monica J., Kalinichenko Vladimir V., Gambin Anna, Belmont John, Stankiewicz Pawel, Comparative Analyses of Lung Transcriptomes in Patients with Alveolar Capillary Dysplasia with Misalignment of Pulmonary Veins and in Foxf1 Heterozygous Knockout Mice, 10.1371/journal.pone.0094390
  45. Stankiewicz Paweł, Sen Partha, Bhatt Samarth S., Storer Mekayla, Xia Zhilian, Bejjani Bassem A., Ou Zhishuo, Wiszniewska Joanna, Driscoll Daniel J., Bolivar Juan, Bauer Mislen, Zackai Elaine H., McDonald-McGinn Donna, Nowaczyk Małgorzata M.J., Murray Mitzi, Shaikh Tamim H., Martin Vicki, Tyreman Matthew, Simonic Ingrid, Willatt Lionel, Paterson Joan, Mehta Sarju, Rajan Diana, Fitzgerald Tomas, Gribble Susan, Prigmore Elena, Patel Ankita, Shaffer Lisa G., Carter Nigel P., Cheung Sau Wai, Langston Claire, Shaw-Smith Charles, Genomic and Genic Deletions of the FOX Gene Cluster on 16q24.1 and Inactivating Mutations of FOXF1 Cause Alveolar Capillary Dysplasia and Other Malformations, 10.1016/j.ajhg.2009.05.005
  46. Reiter Joel, Szafranski Przemyslaw, Breuer Oded, Perles Zeev, Dagan Tamir, Stankiewicz Paweł, Kerem Eitan, Variable phenotypic presentation of a novelFOXF1missense mutation in a single family : Variable Phenotype of a Novel FOXF1 Mutation, 10.1002/ppul.23425
  47. Szafranski P., Dharmadhikari A. V., Brosens E., Gurha P., Kolodziejska K. E., Zhishuo O., Dittwald P., Majewski T., Mohan K. N., Chen B., Person R. E., Tibboel D., de Klein A., Pinner J., Chopra M., Malcolm G., Peters G., Arbuckle S., Guiang S. F., Hustead V. A., Jessurun J., Hirsch R., Witte D. P., Maystadt I., Sebire N., Fisher R., Langston C., Sen P., Stankiewicz P., Small noncoding differentially methylated copy-number variants, including lncRNA genes, cause a lethal lung developmental disorder, 10.1101/gr.141887.112
  48. Szafranski Przemyslaw, Yang Yaping, Nelson Melissa U., Bizzarro Matthew J., Morotti Raffaella A., Langston Claire, Stankiewicz Paweł, NovelFOXF1Deep Intronic Deletion Causes Lethal Lung Developmental Disorder, Alveolar Capillary Dysplasia with Misalignment of Pulmonary Veins, 10.1002/humu.22395
  49. Szafranski Przemyslaw, Dharmadhikari Avinash V., Wambach Jennifer A., Towe Chris T., White Frances V., Grady R. Mark, Eghtesady Pirooz, Cole F. Sessions, Deutsch Gail, Sen Partha, Stankiewicz Paweł, Two deletions overlapping a distantFOXF1enhancer unravel the role of lncRNALINC01081in etiology of alveolar capillary dysplasia with misalignment of pulmonary veins, 10.1002/ajmg.a.36606
  50. Tasha Ilir, Brook Rachel, Frasure Heidi, Lazebnik Noam, Prenatal Detection of Cardiac Anomalies in Fetuses with Single Umbilical Artery: Diagnostic Accuracy Comparison of Maternal-Fetal-Medicine and Pediatric Cardiologist, 10.1155/2014/265421
  51. Warzecha Claude C., Sato Trey K., Nabet Behnam, Hogenesch John B., Carstens Russ P., ESRP1 and ESRP2 Are Epithelial Cell-Type-Specific Regulators of FGFR2 Splicing, 10.1016/j.molcel.2009.01.025
  52. Yong P.J., Marion S.A., Barrett I.J., Kalousek D.K., Robinson W.P., Evidence for imprinting on chromosome 16: The effect of uniparental disomy on the outcome of mosaic trisomy 16 pregnancies, 10.1002/ajmg.10702
  53. Yu Shihui, Shao Lei, Kilbride Howard, Zwick David L., Haploinsufficiencies ofFOXF1andFOXC2genes associated with lethal alveolar capillary dysplasia and congenital heart disease, 10.1002/ajmg.a.33378
  54. Zufferey Flore, Martinet Danielle, Osterheld Maria-Chiara, Niel-Bütschi Florence, Giannoni Eric, Schmutz Nathalie Besuchet, Xia Zhilian, Beckmann Jacques S., Shaw-Smith Charles, Stankiewicz Pawel, Langston Claire, Fellmann Florence, 16q24.1 microdeletion in a premature newborn: Usefulness of array-based comparative genomic hybridization in persistent pulmonary hypertension of the newborn : , 10.1097/pcc.0b013e3182192c96
Bibliographic reference Szafranski, Przemyslaw ; Gambin, Tomasz ; Dharmadhikari, Avinash V ; Akdemir, Kadir Caner ; Jhangiani, Shalini N ; et. al. Pathogenetics of alveolar capillary dysplasia with misalignment of pulmonary veins.. In: Human Genetics, Vol. 135, no.5, p. 569-586 (2016)
Permanent URL http://hdl.handle.net/2078.1/184743