Prenatal and infantile diagnosis of craniosynostosis in individuals with RASopathies.
Cardiofaciocutaneous syndrome
Noonan syndrome
RASopathy
craniosynostosis
infantile
prenatal
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:
29 Sep 2023
29 Sep 2023
Historique:
revised:
22
08
2023
received:
27
06
2023
accepted:
25
08
2023
pubmed:
29
9
2023
medline:
29
9
2023
entrez:
29
9
2023
Statut:
aheadofprint
Résumé
Fetuses with RASopathies can have a wide variety of anomalies including increased nuchal translucency, hydrops fetalis, and structural anomalies (typically cardiac and renal). There are few reports that describe prenatal-onset craniosynostosis in association with a RASopathy diagnosis. We present clinical and molecular characteristics of five individuals with RASopathy and craniosynostosis. Two were diagnosed with craniosynostosis prenatally, 1 was diagnosed as a neonate, and 2 had evidence of craniosynostosis noted as neonates without formal diagnosis until later. Two of these individuals have Noonan syndrome (PTPN11 and KRAS variants) and three individuals have Cardiofaciocutaneous syndrome (KRAS variants). Three individuals had single suture synostosis and two had multiple suture involvement. The most common sutures involved were sagittal (n = 3), followed by coronal (n = 3), and lambdoid (n = 2) sutures. This case series confirms craniosynostosis as one of the prenatal findings in individuals with RASopathies and emphasizes the importance of considering a RASopathy diagnosis in fetuses with multiple anomalies in combination with craniosynostosis.
Identifiants
pubmed: 37774117
doi: 10.1002/ajmg.a.63397
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023 The Authors. American Journal of Medical Genetics Part A published by Wiley Periodicals LLC.
Références
Addissie, Y. A., Kotecha, U., Hart, R. A., Martinez, A. F., Kruszka, P., & Muenke, M. (2015). Craniosynostosis and Noonan syndrome with KRAS mutations: Expanding the phenotype with a case report and review of the literature. American Journal of Medical Genetics. Part A, 167A(11), 2657-2663. https://doi.org/10.1002/ajmg.a.37259
Bertola, D., Yamamoto, G., Buscarilli, M., Jorge, A., Passos-Bueno, M. R., & Kim, C. (2017). The recurrent PPP1CB mutation p.Pro49Arg in an additional Noonan-like syndrome individual: Broadening the clinical phenotype. American Journal of Medical Genetics Part A, 173A, 824-828. https://doi.org/10.1002/ajmg.a.38070
Biard, J. M., Steenhaut, P., Bernard, P., Race, V., & Sznajer, Y. (2019). Antenatal diagnosis of cardio-facio-cutaneous syndrome: Prenatal characteristics and contribution of fetal facial dysmorphic signs in utero. About a case and review of literature. European Journal of Obstetrics, Gynecology, and Reproductive Biology, 240, 232-241. https://doi.org/10.1016/j.ejogrb.2019.06.035
Boulet, S. L., Rasmussen, S. A., & Honein, M. A. (2008). A population-based study of craniosynostosis in metropolitan Atlanta, 1989-2003. American Journal of Medical Genetics. Part A, 146A(8), 984-991. https://doi.org/10.1002/ajmg.a.32208
Brasil, A. S., Malaquias, A. C., Kim, C. A., Krieger, J. E., Jorge, A. A., Pereira, A. C., & Bertola, D. R. (2012). KRAS gene mutations in Noonan syndrome familial cases cluster in the vicinity of the switch II region of the G-domain: Report of another family with metopic craniosynostosis. American Journal of Medical Genetics. Part A, 158A(5), 1178-1184. https://doi.org/10.1002/ajmg.a.35270
Cunningham, M. L., Seto, M. L., Ratisoontorn, C., Heike, C. L., & Hing, A. V. (2007). Syndromic craniosynostosis: From history to hydrogen bonds. Orthodontics & Craniofacial Research, 10(2), 67-81. https://doi.org/10.1111/j.1601-6343.2007.00389.x
Davis, A. A., Zuccoli, G., Haredy, M. M., Losee, J., Pollack, I. F., Madan-Khetarpal, S., Goldstein, J. A., & Nischal, K. K. (2019). RASopathy in patients with isolated sagittal synostosis. Global Pediatric Health, 6, 2333794X19846774. https://doi.org/10.1177/2333794X19846774
Gripp, K. W., Aldinger, K. A., Bennett, J. T., Baker, L., Tusi, J., Powell-Hamilton, N., Stabley, D., Sol-Church, K., Timms, A. E., & Dobyns, W. B. (2016). A novel rasopathy caused by recurrent de novo missense mutations in PPP1CB closely resembles Noonan syndrome with loose anagen hair. American Journal of Medical Genetics. Part A, 170(9), 2237-2247. https://doi.org/10.1002/ajmg.a.37781
Hebron, K. E., Hernandez, E. R., & Yohe, M. E. (2022). The RASopathies: From pathogenetics to therapeutics. Disease Models and Mechanisms, 15(2), dmm049107. https://doi.org/10.1242/dmm.049107
Jezela-Stanek, A., & Krajewska-Walasek, M. (2013). Genetic causes of syndromic craniosynostoses. European Journal of Paediatric Neurology, 17(3), 221-224. https://doi.org/10.1016/j.ejpn.2012.09.009
Johnson, D., & Wilkie, A. O. (2011). Craniosynostosis. European Journal of Human Genetics, 19(4), 369-376. https://doi.org/10.1038/ejhg.2010.235
Kim, H. J., Lee, M. H., Park, H. S., Park, M. H., Lee, S. W., Kim, S. Y., Choi, J. Y., Shin, H. I., Kim, H. J., & Ryoo, H. M. (2003). Erk pathway and activator protein 1 play crucial roles in FGF2-stimulated premature cranial suture closure. Developmental Dynamics, 227(3), 335-346. https://doi.org/10.1002/dvdy.10319
Kimonis, V., Gold, J. A., Hoffman, T. L., Panchal, J., & Boyadjiev, S. A. (2007). Genetics of craniosynostosis. Seminars in Pediatric Neurology, 14(3), 150-161. https://doi.org/10.1016/j.spen.2007.08.008
Kratz, C. P., Zampino, G., Kriek, M., Kant, S. G., Leoni, C., Pantaleoni, F., Oudesluys-Murphy, A. M., Di Rocco, C., Kloska, S. P., Tartaglia, M., & Zenker, M. (2009). Craniosynostosis in patients with Noonan syndrome caused by germline KRAS mutations. American Journal of Medical Genetics. Part A, 149A(5), 1036-1040. https://doi.org/10.1002/ajmg.a.32786
Lo, F. S., Lin, J. L., Kuo, M. T., Chiu, P. C., Shu, S. G., Chao, M. C., Lee, Y. J., & Lin, S. P. (2009). Noonan syndrome caused by germline KRAS mutation in Taiwan: Report of two patients and a review of the literature. European Journal of Pediatrics, 168(8), 919-923. https://doi.org/10.1007/s00431-008-0858-z
Mangels, R., Blumenfeld, Y. J., Homeyer, M., Mrazek-Pugh, B., Hintz, S. R., & Hudgins, L. (2021). RASopathies: A significant cause of polyhydramnios? Prenatal Diagnosis, 41(3), 362-367. https://doi.org/10.1002/pd.5862
McDonald, B. S., Pigors, M., Kelsell, D. P., O'Toole, E. A., Burkitt-Wright, E., Kerr, B., & Batta, K. (2018). Noonan syndrome with multiple lentigines and associated craniosynostosis. Clinical and Experimental Dermatology, 43(3), 357-359. https://doi.org/10.1111/ced.13329
Motta, M., Fasano, G., Gredy, S., Brinkmann, J., Bonnard, A. A., Simsek-Kiper, P. O., Gulec, E. Y., Essaddam, L., Utine, G. E., Guarnetti Prandi, I., Venditti, M., Pantaleoni, F., Radio, F. C., Ciolfi, A., Petrini, S., Consoli, F., Vignal, C., Hepbasli, D., Ullrich, M., … Tartaglia, M. (2021). SPRED2 loss-of-function causes a recessive Noonan syndrome-like phenotype. American Journal of Human Genetics, 108(11), 2112-2129. https://doi.org/10.1016/j.ajhg.2021.09.007
Myers, A., Bernstein, J. A., Brennan, M. L., Curry, C., Esplin, E. D., Fisher, J., Homeyer, M., Manning, M. A., Muller, E. A., Niemi, A. K., Seaver, L. H., Hintz, S. R., & Hudgins, L. (2014). Perinatal features of the RASopathies: Noonan syndrome, cardiofaciocutaneous syndrome and Costello syndrome. American Journal of Medical Genetics. Part A, 164A(11), 2814-2821. https://doi.org/10.1002/ajmg.a.36737
Nagai, K., Niihori, T., Okamoto, N., Kondo, A., Suga, K., Ohhira, T., Hayabuchi, Y., Homma, Y., Nakagawa, R., Ifuku, T., Abe, T., Mizuguchi, T., Matsumoto, N., & Aoki, Y. (2021). Duplications in the G3 domain or switch II region in HRAS identified in patients with Costello syndrome. Human Mutation, 43(1), 3-15. Portico. https://doi.org/10.1002/humu.24287
Rauen, K. A. (2013). The RASopathies. Annual Review of Genomics and Human Genetics, 14, 355-369. https://doi.org/10.1146/annurev-genom-091212-153523
Rodriguez, F., Ponce, D., Berward, F. J., Lopetegui, B., Cassorla, F., & Aracena, M. (2019). RAF1 variant in a patient with Noonan syndrome with multiple lentigines and craniosynostosis. American Journal of Medical Genetics. Part A, 179(8), 1598-1602. https://doi.org/10.1002/ajmg.a.61203
Schubbert, S., Zenker, M., Rowe, S. L., Böll, S., Klein, C., Bollag, G., van der Burgt, I., Musante, L., Kalscheuer, V., Wehner, L. E., Nguyen, H., West, B., Zhang, K. Y., Sistermans, E., Rauch, A., Niemeyer, C. M., Shannon, K., & Kratz, C. P. (2006). Germline KRAS mutations cause Noonan syndrome. Nature Genetics, 38, 331-336. https://doi.org/10.1038/ng1748
Shukla, V., Coumoul, X., Wang, R. H., Kim, H. S., & Deng, C. X. (2007). RNA interference and inhibition of MEK-ERK signaling prevent abnormal skeletal phenotypes in a mouse model of craniosynostosis. Nature Genetics, 39(9), 1145-1150. https://doi.org/10.1038/ng2096
Sparks, T. N., Lianoglou, B. R., Adami, R. R., Pluym, I. D., Holliman, K., Duffy, J., Downum, S. L., Patel, S., Faubel, A., Boe, N. M., Field, N. T., Murphy, A., Laurent, L. C., Jolley, J., Uy, C., Slavotinek, A. M., Devine, P., Hodoglugil, U., Van Ziffle, J., … University of California Fetal-Maternal Consortium; University of California, San Francisco Center for Maternal-Fetal Precision Medicine. (2020). Exome sequencing for prenatal diagnosis in nonimmune hydrops fetalis. New England Journal of Medicine, 383(18), 1746-1756. https://doi.org/10.1056/NEJMoa2023643
Stuurman, K. E., Joosten, M., van der Burgt, I., Elting, M., Yntema, H. G., Meijers-Heijboer, H., & Rinne, T. (2019). Prenatal ultrasound findings of rasopathies in a cohort of 424 fetuses: Update on genetic testing in the NGS era. Journal of Medical Genetics, 56(10), 654-661. https://doi.org/10.1136/jmedgenet-2018-105746
Takenouchi, T., Sakamoto, Y., Miwa, T., Torii, C., Kosaki, R., Kishi, K., Takahashi, T., & Kosaki, K. (2014). Severe craniosynostosis with Noonan syndrome phenotype associated with SHOC2 mutation: Clinical evidence of crosslink between FGFR and RAS signaling pathways. American Journal of Medical Genetics. Part A, 164A(11), 2869-2872. https://doi.org/10.1002/ajmg.a.36705
Tartaglia, M., Aoki, Y., & Gelb, B. D. (2022). The molecular genetics of RASopathies: An update on novel disease genes and new disorders. American Journal of Medical Genetics. Part C, Seminars in Medical Genetics, 190(4), 425-439. https://doi.org/10.1002/ajmg.c.32012
Tartaglia, M., & Gelb, B. D. (2010). Disorders of dysregulated signal traffic through the RAS-MAPK pathway: Phenotypic spectrum and molecular mechanisms. Annals of the New York Academy of Sciences, 1214, 99-121. https://doi.org/10.1111/j.1749-6632.2010.05790.x
Tidyman, W. E., & Rauen, K. A. (2016). Expansion of the RASopathies. Current Genetic Medicine Reports, 4(3), 57-64. https://doi.org/10.1007/s40142-016-0100-7
Timberlake, A. T., & Persing, J. A. (2018). Genetics of nonsyndromic craniosynostosis. Plastic and Reconstructive Surgery, 141(6), 1508-1516. https://doi.org/10.1097/PRS.0000000000004374
Twigg, S. R., Vorgia, E., McGowan, S. J., Peraki, I., Fenwick, A. L., Sharma, V. P., Allegra, M., Zaragkoulias, A., Sadighi Akha, E., Knight, S. J., Lord, H., Lester, T., Izatt, L., Lampe, A. K., Mohammed, S. N., Stewart, F. J., Verloes, A., Wilson, L. C., Healy, C., … Wilkie, A. O. (2013). Reduced dosage of ERF causes complex craniosynostosis in humans and mice and links ERK1/2 signaling to regulation of osteogenesis. Nature Genetics, 45(3), 308-313. https://doi.org/10.1038/ng.2539
Twigg, S. R., & Wilkie, A. O. (2015). A genetic-pathophysiological framework for craniosynostosis. American Journal of Human Genetics, 97(3), 359-377. https://doi.org/10.1016/j.ajhg.2015.07.006
Ueda, K., Yaoita, M., Niihori, T., Aoki, Y., & Okamoto, N. (2017). Craniosynostosis in patients with RASopathies: Accumulating clinical evidence for expanding the phenotype. American Journal of Medical Genetics. Part A, 173(9), 2346-2352. https://doi.org/10.1002/ajmg.a.38337
Viskochil, D. H. (2011). Disorders of the Ras pathway: An introduction. American Journal of Medical Genetics. Part C, Seminars in Medical Genetics, 157C(2), 79-82. https://doi.org/10.1002/ajmg.c.30301
Weaver, K. N., Care, M., Wakefield, E., Zarate, Y. A., Skoch, J., Gripp, K. W., & Prada, C. E. (2022). Craniosynostosis is a feature of Costello syndrome. American Journal of Medical Genetics. Part A, 188(4), 1280-1286. https://doi.org/10.1002/ajmg.a.62620
Zenker, M. (2022). Clinical overview on RASopathies. American Journal of Medical Genetics. Part C, Seminars in Medical Genetics, 190(4), 414-424. https://doi.org/10.1002/ajmg.c.32015
Zollino, M., Lattante, S., Orteschi, D., Frangella, S., Doronzio, P. N., Contaldo, I., Mercuri, E., & Marangi, G. (2017). Syndromic craniosynostosis can define new candidate genes for suture development or result from the non-specific effects of pleiotropic genes: Rasopathies and Chromatinopathies as examples. Frontiers in Neuroscience, 11, 587. https://doi.org/10.3389/fnins.2017.00587