Toward clinical and molecular dissection of frontonasal dysplasia with facial skin polyps: From Pai syndrome to differential diagnosis through a series of 27 patients.


Journal

American journal of medical genetics. Part A
ISSN: 1552-4833
Titre abrégé: Am J Med Genet A
Pays: United States
ID NLM: 101235741

Informations de publication

Date de publication:
07 2022
Historique:
revised: 20 10 2021
received: 30 04 2021
accepted: 02 11 2021
pubmed: 22 4 2022
medline: 15 6 2022
entrez: 21 4 2022
Statut: ppublish

Résumé

Unique or multiple congenital facial skin polyps are features of several rare syndromes, from the most well-known Pai syndrome (PS), to the less recognized oculoauriculofrontonasal syndrome (OAFNS), encephalocraniocutaneous lipomatosis (ECCL), or Sakoda complex (SC). We set up a research project aiming to identify the molecular bases of PS. We reviewed 27 individuals presenting with a syndromic frontonasal polyp and initially referred for PS. Based on strict clinical classification criteria, we could confirm only nine (33%) typical and two (7%) atypical PS individuals. The remaining ones were either OAFNS (11/27-41%) or presenting with an overlapping syndrome (5/27-19%). Because of the phenotypic overlap between these entities, OAFNS, ECCL, and SC can be either considered as differential diagnosis of PS or part of the same spectrum. Exome and/or genome sequencing from blood DNA in 12 patients and from affected tissue in one patient failed to identify any replication in candidate genes. Taken together, our data suggest that conventional approaches routinely utilized for the identification of molecular etiologies responsible for Mendelian disorders are inconclusive. Future studies on affected tissues and multiomics studies will thus be required in order to address either the contribution of mosaic or noncoding variation in these diseases.

Identifiants

pubmed: 35445792
doi: 10.1002/ajmg.a.62739
doi:

Types de publication

Journal Article Review Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2036-2047

Informations de copyright

© 2022 Wiley Periodicals LLC.

Références

Adolphs, N., Arnaud, E., Haberl, E.-J., Graul-Neumann, L., Schmidt, G., Menneking, H., & Hoffmeister, B. (2012). The oculo-auriculo-fronto-nasal syndrome (OAFNS) - Description of a rare and complex craniofacial deformity and its interdisciplinary management before school age. Journal of Cranio-Maxillofacial Surgery: Official Publication of European Association for Cranio-Maxillofacial Surgery, 40, 668-674.
Al-Mazrou, K. A., Al-Rekabi, A., Alorainy, I. A., Al-Kharfi, T., & Al-Serhani, A. M. (2001). Pai syndrome: A report of a case and review of the literature. International Journal of Pediatric Otorhinolaryngology, 61, 149-153.
Bennett, J. T., Tan, T. Y., Alcantara, D., Tetrault, M., Timms, A. E., Jensen, D., Collins, S., Nowaczyk, M. J. M., Lindhurst, M. J., Christensen, K. M., Braddock, S. R., Brandling-Bennett, H., Hennekam, R. C. M., Chung, B., Lehman, A., Su, J., Ng, S., Amor, D. J., Majewski, J., … McDonell, L. M. (2016). Mosaic activating mutations in FGFR1 cause encephalocraniocutaneous lipomatosis. American Journal of Human Genetics, 98, 579-587.
Boppudi, S., Bogershausen, N., Hove, H. B., Percin, E. F., Aslan, D., Dvorsky, R., Kayhan, G., Li, Y., Cursiefen, C., Tantcheva-Poor, I., Toft, P. B., Bartsch, O., Lissewski, C., Wieland, I., Jakubiczka, S., Wollnik, B., Ahmadian, M. R., Heindl, L. M., & Zenker, M. (2016). Specific mosaic KRAS mutations affecting codon 146 cause oculoectodermal syndrome and encephalocraniocutaneous lipomatosis. Clinical Genetics, 90, 334-342.
Borumandi, F., Chadha, A., Dediol, E., & Uglesic, V. (2015). A diagnostic conundrum: Ectopic nasal ossification, submucosal alveolar cleft, absent posterior atlantal arch, and corpus callosum lipoma. The Cleft Palate-Craniofacial Journal: Official Publication of the American Cleft Palate-Craniofacial Association, 52, 761-765.
Carey, J., & Yong, S. (1981). Frontonasal dysplasia and the Goldenhar syndrome: The oculo-auriculo-frontonasal syndrome.
Casey, H. D., Braddock, S. R., Haskins, R. C., Carey, J. C., & Morales, L. J. (1996). Frontonasal malformation and the oculoauriculovertebral spectrum: The oculoauriculofrontonasal syndrome. The Cleft Palate-Craniofacial Journal: Official Publication of the American Cleft Palate-Craniofacial Association, 33, 519-523.
Chousta, A., Ville, D., James, I., Foray, P., Bisch, C., Depardon, P., Rudigoz, R.-C., & Guibaud, L. (2008). Pericallosal lipoma associated with Pai syndrome: Prenatal imaging findings. Ultrasound in Obstetrics & Gynecology: The Official Journal of the International Society of Ultrasound in Obstetrics and Gynecology, 32, 708-710.
Coban, Y. K., Boran, C., Omeroglu, S. A., & Okur, E. (2003). Pai syndrome: An adult patient with bifid nose and frontal hairline marker. The Cleft Palate-Craniofacial Journal: Official Publication of the American Cleft Palate-Craniofacial Association, 40, 325-328.
de Boutray, M., Beziat, J.-L., Yachouh, J., Bigorre, M., Gleizal, A., & Captier, G. (2016). Median cleft of the upper lip: A new classification to guide treatment decisions. Journal of Cranio-Maxillofacial Surgery: Official Publication of European Association for Cranio-Maxillofacial Surgery, 44, 664-671.
Evans, K. N., Gruss, J. S., Khanna, P. C., Cunningham, M. L., Cox, T. C., & Hing, A. V. (2013). Oculoauriculofrontonasal syndrome: Case series revealing new bony nasal anomalies in an old syndrome. American Journal of Medical Genetics. Part A, 161A, 1345-1353.
Farlie, P. G., Baker, N. L., Yap, P., & Tan, T. Y. (2016). Frontonasal dysplasia: Towards an understanding of molecular and developmental aetiology. Molecular Syndromology, 7, 312-321.
Giffoni, S. D. A., Cendes, F., Valente, M., & Gil-da-Silva-Lopes, V. L. (2010). Malformations of cortical development in patients with midline facial defects and ocular hypertelorism. The Cleft Palate-Craniofacial Journal: Official Publication of the American Cleft Palate-Craniofacial Association, 47, 343-351.
Gilissen, C., Hehir-Kwa, J. Y., Thung, D. T., van de Vorst, M., van Bon, B. W. M., Willemsen, M. H., Kwint, M., Janssen, I. M., Hoischen, A., Schenck, A., Leach, R., Klein, R., Tearle, R., Bo, T., Pfundt, R., Yntema, H. G., de Vries, B. B. A., Kleefstra, T., Brunner, H. G., … Veltman, J. A. (2014). Genome sequencing identifies major causes of severe intellectual disability. Nature, 511(7509), 344-347. https://doi.org/10.1038/nature13394
Guion-Almeida, M. L., Mellado, C., Beltran, C., & Richieri-Costa, A. (2007). Pai syndrome: Report of seven South American patients. American Journal of Medical Genetics. Part A, 143A, 3273-3279.
Guion-Almeida, M. L., & Richieri-Costa, A. (2009). Severe midline craniofacial anomalies: Overlap with Pai syndrome. Clinical Dysmorphology, 18, 154-157.
Iwata, J., Hacia, J. G., Suzuki, A., Sanchez-Lara, P. A., Urata, M., & Chai, Y. (2012). Modulation of noncanonical TGF-beta signaling prevents cleft palate in Tgfbr2 mutant mice. The Journal of Clinical Investigation, 122, 873-885.
Le Lievre, C. S., & Le Douarin, N. M. (1975). Mesenchymal derivatives of the neural crest: Analysis of chimaeric quail and chick embryos. Journal of Embryology and Experimental Morphology, 34, 125-154.
Lederer, D., Wilson, B., Lefesvre, P., Poorten, V. V., Kirkham, N., Mitra, D., Verellen-Dumoulin, C., & Devriendt, K. (2012). Atypical findings in three patients with Pai syndrome and literature review. American Journal of Medical Genetics. Part A, 158A, 2899-2904.
Lees, M. M., Connelly, F., Kangesu, L., Sommerlad, B., & Barnicoat, A. (2006). Midline cleft lip and nasal dermoids over five generations: A distinct entity or autosomal dominant Pai syndrome? Clinical Dysmorphology, 15, 155-159.
Lees, M. M., Hodgkins, P., Reardon, W., Taylor, D., Stanhope, R., Jones, B., Hayward, R., Hockley, A. D., Baraitser, M., & Winter, R. M. (1998). Frontonasal dysplasia with optic disc anomalies and other midline craniofacial defects: A report of six cases. Clinical Dysmorphology, 7, 157-162.
Lehalle, D., Altunoglu, U., Bruel, A.-L., Assoum, M., Duffourd, Y., Masurel, A., Baujat, G., Bessieres, B., Captier, G., Edery, P., Elcioglu, N. H., Genevieve, D., Goldenberg, A., Heron, D., Grotto, S., Marlin, S., Putoux, A., Rossi, M., Saugier-Veber, P., … Faivre, L. (2018). The oculoauriculofrontonasal syndrome: Further clinical characterization and additional evidence suggesting a nontraditional mode of inheritance. American Journal of Medical Genetics. Part A, 176, 2740-2750.
Lies, S., Beckwith, T., Mills, J., Butler, L., Ezaki, M., & Oishi, S. (2019). Case series: Amniotic band sequence with craniofacial abnormalities. Birth Defects Research, 111, 1494-1500.
Magdalene, D., Kalita, L., Deka, A., & Deka, A. C. (2010). Mid line craniofacial defects and morning glory disc anomaly with clinical anophthalmos-A distinct clinical entity. Orbit (Amsterdam, Netherlands), 29, 57-59.
Messler, S., Kropp, S., Episkopou, V., Felici, A., Wurthner, J., Lemke, R., Jerabek-Willemsen, M., Willecke, R., Scheu, S., Pfeffer, K., & Wurthner, J. U. (2011). The TGF-beta signaling modulators TRAP1/TGFBRAP1 and VPS39/Vam6/TLP are essential for early embryonic development. Immunobiology, 216, 343-350.
Moog, U. (2009). Encephalocraniocutaneous lipomatosis. Journal of Medical Genetics, 46, 721-729.
Morice, A., Galliani, E., Amiel, J., Rachwalski, M., Neiva, C., Thauvin-Robinet, C., Vazquez, M.-P., Picard, A., & Kadlub, N. (2019). Diagnostic criteria in Pai syndrome: Results of a case series and a literature review. International Journal of Oral and Maxillofacial Surgery, 48, 283-290.
Musarella, M. A., & Young, I. D. (1986). A patient with median cleft face anomaly and bilateral Goldenhar anomaly. American Journal of Medical Genetics. Supplement, 2, 135-141.
Pai, G. S., Levkoff, A. H., & Leithiser, R. E. J. (1987). Median cleft of the upper lip associated with lipomas of the central nervous system and cutaneous polyps. American Journal of Medical Genetics, 26, 921-924.
Richieri-Costa, A., & Guion-Almeida, M. L. (2004). The syndrome of frontonasal dysplasia, callosal agenesis, basal encephalocele, and eye anomalies - Phenotypic and aetiological considerations. International Journal of Medical Sciences, 1, 34-42.
Roman Corona-Rivera, J., Lopez-Marure, E., Gomez-Ruiz, L., del Carmen, A.-F. M., Quezada-Lopez, C., Perez-Molina, J., & Santibanez-Escobar, L. P. (2007). Airway anomalies in the oculoauriculofrontonasal syndrome. Clinical Dysmorphology, 16, 43-45.
Romero-Valdovinos, M., Galvan-Montano, A., Olivo-Diaz, A., Maravilla, P., Bobadilla, N. A., Vadillo-Ortega, F., & Flisser, A. (2015). The amniotic band syndrome in the rat is associated with the activation of transforming growth factor-beta. The American Journal of Pathology, 185, 2076-2082.
Rudnik-Schoneborn, S., & Zerres, K. (1994). A further patient with Pai syndrome with autosomal dominant inheritance? Journal of Medical Genetics, 31, 497-498.
Savasta, S., Chiapedi, S., Perrini, S., Tognato, E., Corsano, L., & Chiara, A. (2008). Pai syndrome: A further report of a case with bifid nose, lipoma, and agenesis of the corpus callosum. Child's Nervous System: ChNS: Official Journal of the International Society for Pediatric Neurosurgery, 24, 773-776.
Schrander-Stumpel, C. T., de Die-Smulders, C. E., Hennekam, R. C., Fryns, J. P., Bouckaert, P. X., Brouwer, O. F., da Costa, J. J., Lommen, E. J., & Maaswinkel-Mooy, P. D. (1992). Oculoauriculovertebral spectrum and cerebral anomalies. Journal of Medical Genetics, 29, 326-331.
Suzuki, A., Sangani, D. R., Ansari, A., & Iwata, J. (2016). Molecular mechanisms of midfacial developmental defects. Developmental Dynamics: Official Publication of the American Association for Anatomy, 245, 276-293.
Szeto, C., Tewfik, T. L., Jewer, D., & Rideout, A. (2005). Pai syndrome (median cleft palate, cutaneous nasal polyp, and midline lipoma of the corpus callosum): A case report and literature review. International Journal of Pediatric Otorhinolaryngology, 69, 1247-1252.
Vaccarella, F., Pini Prato, A., Fasciolo, A., Pisano, M., Carlini, C., & Seymandi, P. L. (2008). Phenotypic variability of Pai syndrome: Report of two patients and review of the literature. International Journal of Oral and Maxillofacial Surgery, 37, 1059-1064.
Vendramini-Pittoli, S., Guion-Almeida, M. L., Santos, J. M., Garcia Junior, S. M., Yoshida, M. M., Richieri-Costa, A., & Kokitsu-Nakata, N. M. (2015). An unusual presentation of oculoauriculovertebral spectrum with a Tessier 30 cleft: Report on two cases. Clinical Dysmorphology, 24, 144-150.

Auteurs

Daphné Lehalle (D)

Centre de Génétique et Centre de Référence Anomalies du Développement et Syndromes Malformatifs de l'Interrégion Est, FHU TRANSLAD, Centre Hospitalier Universitaire Dijon, Dijon, France.
Equipe GAD, INSERM LNC UMR 1231, FHU TRANSLAD, Faculté de Médecine, Université de Bourgogne Franche-Comté, Dijon, France.
Unité Fonctionnelle d'Innovation diagnostique des maladies rares, Pôle de Biologie, FHU-TRANSLAD, CHU Dijon Bourgogne, Dijon, France.
Département de Génétique, AP-HP, Hôpital de la Pitié-Salpêtrière, Paris, France.

Ange-Line Bruel (AL)

Equipe GAD, INSERM LNC UMR 1231, FHU TRANSLAD, Faculté de Médecine, Université de Bourgogne Franche-Comté, Dijon, France.
Unité Fonctionnelle d'Innovation diagnostique des maladies rares, Pôle de Biologie, FHU-TRANSLAD, CHU Dijon Bourgogne, Dijon, France.

Antonio Vitobello (A)

Equipe GAD, INSERM LNC UMR 1231, FHU TRANSLAD, Faculté de Médecine, Université de Bourgogne Franche-Comté, Dijon, France.
Unité Fonctionnelle d'Innovation diagnostique des maladies rares, Pôle de Biologie, FHU-TRANSLAD, CHU Dijon Bourgogne, Dijon, France.

Anne-Sophie Denommé-Pichon (AS)

Equipe GAD, INSERM LNC UMR 1231, FHU TRANSLAD, Faculté de Médecine, Université de Bourgogne Franche-Comté, Dijon, France.
Unité Fonctionnelle d'Innovation diagnostique des maladies rares, Pôle de Biologie, FHU-TRANSLAD, CHU Dijon Bourgogne, Dijon, France.

Yannis Duffourd (Y)

Equipe GAD, INSERM LNC UMR 1231, FHU TRANSLAD, Faculté de Médecine, Université de Bourgogne Franche-Comté, Dijon, France.
Unité Fonctionnelle d'Innovation diagnostique des maladies rares, Pôle de Biologie, FHU-TRANSLAD, CHU Dijon Bourgogne, Dijon, France.

Mirna Assoum (M)

Equipe GAD, INSERM LNC UMR 1231, FHU TRANSLAD, Faculté de Médecine, Université de Bourgogne Franche-Comté, Dijon, France.

Jeanne Amiel (J)

Service de Génétique, INSERM U781, Hôpital Necker-Enfants Malades, Institut Imagine, University Sorbonne-Paris-Cité, Paris, France.

Geneviève Baujat (G)

Service de Génétique, INSERM U781, Hôpital Necker-Enfants Malades, Institut Imagine, University Sorbonne-Paris-Cité, Paris, France.

Bettina Bessieres (B)

Unite d'embryofoetopathologie, Service d'Histologie-Embryologie-Cytogénétique, Hôpital Necker-Enfants Malades APHP, Paris, France.

Stefania Bigoni (S)

UOL of Medical Genetics, Ferrara Hospital University, Ferrara, Italy.

Lydie Burglen (L)

Département de Génétique et Centre de Référence "malformations et maladies congénitales du cervelet," AP-HP, Hôpital Trousseau, Paris, France.

Guillaume Captier (G)

Service de chirurgie orthopédique et plastique pédiatrique, Hôpital Lapeyronie, CHU Montpellier, Montpellier, France.

Rodolphe Dard (R)

Service de Cytogénétique, Centre Hospitalier Intercommunal de Poissy Saint-Germain-en-Laye, Poissy, France.

Patrick Edery (P)

Service de génétique et Centre de Référence des Anomalies du développement de la région Auvergne-Rhône-Alpes, CHU de Lyon, Lyon, France.
Centre de Recherche en Neurosciences de Lyon, INSERM U1028 CNRS UMR 5292, UCB Lyon 1, Villeurbanne, France.

Fernanda Fortunato (F)

UOL of Medical Genetics, Ferrara Hospital University, Ferrara, Italy.

David Geneviève (D)

Genetic Department for Rare Disease and Personalised Medicine, Clinical Division, Montpellier University, Inserm U1183, Montpellier, France.

Alice Goldenberg (A)

Department of Genetics, Rouen University Hospital, Normandy Centre for Genomic and Personalized Medicine, Rouen, France.

Laurent Guibaud (L)

Centre de Recherche en Neurosciences de Lyon, INSERM U1028 CNRS UMR 5292, UCB Lyon 1, Villeurbanne, France.

Delphine Héron (D)

Department of Genetics, Intellectual Disability and Autism Clinical Research Group, Pierre and Marie Curie University, Pitié-Salpêtrière Hospital, Public Hospital Network of Paris, Paris, France.

Muriel Holder-Espinasse (M)

Department of Clinical Genetics, CHU Lille, Lille, France.
Clinical Genetics Department, Guy's Hospital, London, UK.

Damien Lederer (D)

Center for Human Genetics, Institut de Pathologie et Génétique (I.p.G.), Gosselies, Belgium.

Fermina Lopez Grondona (F)

Àrea de Genètica Clínica i Malalties Minoritàries, Hospital Vall d'Hebron, Barcelona, Spain.

Sarah Grotto (S)

Genetic Department for Rare Disease and Personalised Medicine, Clinical Division, Montpellier University, Inserm U1183, Montpellier, France.

Sandrine Marlin (S)

Laboratory of Embryology and Genetics of Malformations, Institut National de la Santé et de la Recherche Médicale (INSERM) UMR 1163, Institut Imagine, Université de Paris, Paris, Spain.

Gwenaël Nadeau (G)

Unité fonctionnelle de cytogénétique, CH de Valence, Valence, France.

Arnaud Picard (A)

Service de Chirurgie Maxillofaciale, Hôpital Necker, Paris, France.

Massimiliano Rossi (M)

Service de Cytogénétique, Centre Hospitalier Intercommunal de Poissy Saint-Germain-en-Laye, Poissy, France.
Service de génétique et Centre de Référence des Anomalies du développement de la région Auvergne-Rhône-Alpes, CHU de Lyon, Lyon, France.

Joëlle Roume (J)

Service de chirurgie orthopédique et plastique pédiatrique, Hôpital Lapeyronie, CHU Montpellier, Montpellier, France.

Damien Sanlaville (D)

Service de Cytogénétique, Centre Hospitalier Intercommunal de Poissy Saint-Germain-en-Laye, Poissy, France.
Service de génétique et Centre de Référence des Anomalies du développement de la région Auvergne-Rhône-Alpes, CHU de Lyon, Lyon, France.

Pascale Saugier-Veber (P)

Department of Genetics, Normandy Centre for Genomic and Personalized Medicine, Normandie Univ, UNIROUEN, Inserm U1245 and Rouen University Hospital, Rouen, France.

Stéphane Triau (S)

Service de Foetopathologie, CHU Angers, Angers, France.

Maria Irene Valenzuela Palafoll (MI)

Àrea de Genètica Clínica i Malalties Minoritàries, Hospital Vall d'Hebron, Barcelona, Spain.

Clémence Vanlerberghe (C)

Department of Clinical Genetics, CHU Lille, Lille, France.

Lionel Van Maldergem (L)

Service de Génétique, CHU Besançon, Besançon, France.

Myriam Vezain (M)

Department of Genetics, Normandy Centre for Genomic and Personalized Medicine, Normandie Univ, UNIROUEN, Inserm U1245 and Rouen University Hospital, Rouen, France.

Catherine Vincent-Delorme (C)

Department of Clinical Genetics, CHU Lille, Lille, France.

Einat Zivi (E)

Medical Genetics Institute, Shaare Zedek Medical Center, Hebrew University of Jerusalem, Jerusalem, Israel.

Julien Thevenon (J)

Centre de Génétique et Centre de Référence Anomalies du Développement et Syndromes Malformatifs de l'Interrégion Est, FHU TRANSLAD, Centre Hospitalier Universitaire Dijon, Dijon, France.
Equipe GAD, INSERM LNC UMR 1231, FHU TRANSLAD, Faculté de Médecine, Université de Bourgogne Franche-Comté, Dijon, France.

Pierre Vabres (P)

Equipe GAD, INSERM LNC UMR 1231, FHU TRANSLAD, Faculté de Médecine, Université de Bourgogne Franche-Comté, Dijon, France.
Service de Dermatologie, CHU Dijon, Dijon, France.

Christel Thauvin-Robinet (C)

Centre de Génétique et Centre de Référence Anomalies du Développement et Syndromes Malformatifs de l'Interrégion Est, FHU TRANSLAD, Centre Hospitalier Universitaire Dijon, Dijon, France.
Equipe GAD, INSERM LNC UMR 1231, FHU TRANSLAD, Faculté de Médecine, Université de Bourgogne Franche-Comté, Dijon, France.
Unité Fonctionnelle d'Innovation diagnostique des maladies rares, Pôle de Biologie, FHU-TRANSLAD, CHU Dijon Bourgogne, Dijon, France.

Patrick Callier (P)

Equipe GAD, INSERM LNC UMR 1231, FHU TRANSLAD, Faculté de Médecine, Université de Bourgogne Franche-Comté, Dijon, France.

Laurence Faivre (L)

Centre de Génétique et Centre de Référence Anomalies du Développement et Syndromes Malformatifs de l'Interrégion Est, FHU TRANSLAD, Centre Hospitalier Universitaire Dijon, Dijon, France.
Equipe GAD, INSERM LNC UMR 1231, FHU TRANSLAD, Faculté de Médecine, Université de Bourgogne Franche-Comté, Dijon, France.
Unité Fonctionnelle d'Innovation diagnostique des maladies rares, Pôle de Biologie, FHU-TRANSLAD, CHU Dijon Bourgogne, Dijon, France.

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