User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Autosomal recessive primary microcephaly due to ASPM mutations: An update

Primary tabs

download
  • Open access
  • PDF
  • 1.42 M
Létard, Pascaline Drunat, Séverine Vial, Yoann Duerinckx, Sarah Ernault, Anais Sznajer, Yves [UCL] Passemard, Sandrine

Autosomal recessive microcephaly or microcephaly primary hereditary (MCPH) is a genetically heterogeneous neurodevelopmental disorder characterized by a reduction in brain volume, indirectly measured by an occipitofrontal circumference (OFC) 2 standard deviations or more below the age- and sex-matched mean (-2SD) at birth and -3SD after 6 months, and leading to intellectual disability of variable severity. The abnormal spindle-like microcephaly gene (ASPM), the human ortholog of the Drosophila melanogaster "abnormal spindle" gene (asp), encodes ASPM, a protein localized at the centrosome of apical neuroprogenitor cells and involved in spindle pole positioning during neurogenesis. Loss-of-function mutations in ASPM cause MCPH5, which affects the majority of all MCPH patients worldwide. Here, we report 47 unpublished patients from 39 families carrying 28 new ASPM mutations, and conduct an exhaustive review of the molecular, clinical, neuroradiological, and neuropsychological features of the 282 families previously reported (with 161 distinct ASPM mutations). Furthermore, we show that ASPM-related microcephaly is not systematically associated with intellectual deficiency and discuss the association between the structural brain defects (strong reduction in cortical volume and surface area) that modify the cortical map of these patients and their cognitive abilities.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2018
Language Anglais
Journal information "Human Mutation" - Vol. 39, no. 3, p. 319-332 (2018)
Peer reviewed yes
Publisher Wiley-Liss ((United States) New York, NY)
issn 1059-7794
e-issn 1098-1004
Publication status Publié
Affiliations UCL - (SLuc) Centre de génétique médicale UCL
UCL - SSS/IREC/SLUC - Pôle St.-Luc
Keywords ASPM ; MCPH ; Brain development ; Brain imaging ; Centrosome ; Intellectual disability ; Primary microcephaly
Links
  1. Abdel-Hamid, Genetic Counseling, 27, 25 (2016a)
  2. Abdel-Hamid Mohamed S., Ismail Manal F., Darwish Hebatallh A., Effat Laila K., Zaki Maha S., Abdel-Salam Ghada M. H., Molecular and phenotypic spectrum ofASPM-related primary microcephaly: Identification of eight novel mutations, 10.1002/ajmg.a.37724
  3. Ahmad I., Baig S. M., Abdulkareem A. R., Hussain M. S., Sur I., Toliat M. R., Nürnberg G., Dalibor N., Moawia A., Waseem S. S., Asif M., Nagra H., Sher M., Khan M. M. A., Hassan I., Rehman S. ur, Thiele H., Altmüller J., Noegel A. A., Nürnberg P., Genetic heterogeneity in Pakistani microcephaly families revisited : Genetic heterogeneity in Pakistani microcephaly families, 10.1111/cge.12955
  4. Akbariazar, Iranian Journal of Child Neurology, 7, 23 (2013)
  5. Al-Gazali Lihadh, Ali Bassam R., Mutations of a country: a mutation review of single gene disorders in the United Arab Emirates (UAE), 10.1002/humu.21232
  6. Ariani F, Mari F, Amitrano S, Di Marco C, Artuso R, Scala E, Meloni I, Della Volpe R, Rossi A, van Bokhoven H, Renieri A, Exome sequencing overrides formal genetics:ASPMmutations in a case study of apparent X-linked microcephalic intellectual deficit : Letter to the Editor, 10.1111/j.1399-0004.2012.01901.x
  7. Bond Jacquelyn, Roberts Emma, Mochida Ganesh H., Hampshire Daniel J., Scott Sheila, Askham Jonathan M., Springell Kelly, Mahadevan Meera, Crow Yanick J., Markham Alexander F., Walsh Christopher A., Woods C. Geoffrey, ASPM is a major determinant of cerebral cortical size, 10.1038/ng995
  8. Bond Jacquelyn, Scott Sheila, Hampshire Daniel J., Springell Kelly, Corry Peter, Abramowicz Marc J., Mochida Ganesh H., Hennekam Raoul C.M., Maher Eamonn R., Fryns Jean-Pierre, Alswaid Abdulrahman, Jafri Hussain, Rashid Yasmin, Mubaidin Ammar, Walsh Christopher A., Roberts Emma, Woods C. Geoffrey, Protein-Truncating Mutations in ASPM Cause Variable Reduction in Brain Size, 10.1086/379085
  9. Bond Jacquelyn, Woods C Geoffrey, Cytoskeletal genes regulating brain size, 10.1016/j.ceb.2005.11.004
  10. Capecchi Mario R., Pozner Amir, ASPM regulates symmetric stem cell division by tuning Cyclin E ubiquitination, 10.1038/ncomms9763
  11. Darvish H., Esmaeeli-Nieh S., Monajemi G. B., Mohseni M., Ghasemi-Firouzabadi S., Abedini S. S., Bahman I., Jamali P., Azimi S., Mojahedi F., Dehghan A., Shafeghati Y., Jankhah A., Falah M., Soltani Banavandi M. J., Ghani-Kakhi M., Garshasbi M., Rakhshani F., Naghavi A., Tzschach A., Neitzel H., Ropers H. H., Kuss A. W., Behjati F., Kahrizi K., Najmabadi H., A clinical and molecular genetic study of 112 Iranian families with primary microcephaly, 10.1136/jmg.2009.076398
  12. Desir Julie, Abramowicz Marc, Tunca Yusuf, Novel mutations in prenatal diagnosis of primary microcephaly, 10.1002/pd.1536
  13. Desir Julie, Cassart Marie, David Philippe, Van Bogaert Patrick, Abramowicz Marc, Primary microcephaly with ASPM mutation shows simplified cortical gyration with antero-posterior gradient pre- and post-natally, 10.1002/ajmg.a.32312
  14. Fish J. L., Kosodo Y., Enard W., Paabo S., Huttner W. B., Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells, 10.1073/pnas.0604066103
  15. Gul Asma, Hassan Muhammad Jawad, Mahmood Saqib, Chen Wenje, Rahmani Safa, Naseer Muhammad Imran, Dellefave Lisa, Muhammad Noor, Rafiq Muhammad Arshad, Ansar Muhammad, Chishti Muhammad Salman, Ali Ghazanfar, Siddique Teepu, Ahmad Wasim, Genetic studies of autosomal recessive primary microcephaly in 33 Pakistani families: novel sequence variants in ASPM gene, 10.1007/s10048-006-0042-4
  16. Gul Asma, Tariq Muhammad, Khan Muhammad Nasim, Hassan Muhammad Jawad, Ali Ghazanfar, Ahmad Wasim, NOVEL PROTEIN-TRUNCATING MUTATIONS IN THEASPMGENE IN FAMILIES WITH AUTOSOMAL RECESSIVE PRIMARY MICROCEPHALY, 10.1080/01677060701508594
  17. Halsall S., Nicholas A. K., Thornton G., Martin H., Geoffrey Woods C., Critical consequences of finding three pathogenic mutations in an individual with recessive disease, 10.1136/jmg.2010.079277
  18. Hashmi Jamil A., Al-Harbi Khalid M., Ramzan Khushnooda, Albalawi Alia M., Mehmood Amir, Samman Mohammed I., Basit Sulman, A novel splice-site mutation in the ASPM gene underlies autosomal recessive primary microcephaly, 10.5144/0256-4947.2016.391
  19. Higgins Julie, Midgley Carol, Bergh Anna-Maria, Bell Sandra M, Askham Jonathan M, Roberts Emma, Binns Ruth K, Sharif Saghira M, Bennett Christopher, Glover David M, Woods C Geoffrey, Morrison Ewan E, Bond Jacquelyn, Human ASPM participates in spindle organisation, spindle orientation and cytokinesis, 10.1186/1471-2121-11-85
  20. Hu Hao, Suckow Vanessa, Musante Luciana, Roggenkamp Viola, Kraemer Nadine, Ropers Hans-Hilger, Hübner Christoph, Wienker Thomas F, Kaindl Angela M, Previously reported new type of autosomal recessive primary microcephaly is caused by compound heterozygousASPMgene mutations, 10.4161/cc.28706
  21. Jamieson C. Ruth, Fryns Jean-Pierre, Jacobs Jos, Matthijs Gert, Abramowicz Marc J., Primary Autosomal Recessive Microcephaly: MCPH5 Maps to 1q25-q32, 10.1086/316909
  22. Kaindl Angela M., Passemard Sandrine, Kumar Pavan, Kraemer Nadine, Issa Lina, Zwirner Angelika, Gerard Benedicte, Verloes Alain, Mani Shyamala, Gressens Pierre, Many roads lead to primary autosomal recessive microcephaly, 10.1016/j.pneurobio.2009.11.002
  23. Komai, American Journal of Human Genetics, 7, 51 (1955)
  24. Kouprina Natalay, Pavlicek Adam, Collins N. Keith, Nakano Megumi, Noskov Vladimir N., Ohzeki Jun-Ichirou, Mochida Ganeshwaran H., Risinger John I., Goldsmith Paul, Gunsior Michelle, Solomon Greg, Gersch William, Kim Jung-Hyun, Barrett J. Carl, Walsh Christopher A., Jurka Jerzy, Masumoto Hiroshi, Larionov Vladimir, The microcephaly ASPM gene is expressed in proliferating tissues and encodes for a mitotic spindle protein, 10.1093/hmg/ddi220
  25. Kouprina Natalay, Pavlicek Adam, Mochida Ganeshwaran H, Solomon Gregory, Gersch William, Yoon Young-Ho, Collura Randall, Ruvolo Maryellen, Barrett J. Carl, Woods C. Geoffrey, Walsh Christopher A, Jurka Jerzy, Larionov Vladimir, Accelerated Evolution of the ASPM Gene Controlling Brain Size Begins Prior to Human Brain Expansion, 10.1371/journal.pbio.0020126
  26. Kousar Rizwana, Nawaz Hira, Khurshid Maryam, Ali Ghazanfer, Khan Saad Ullah, Mir Hina, Ayub Muhammad, Wali Abdul, Ali Nadir, Jelani Musharraf, Basit Sulman, Ahmad Wasim, Ansar Muhammad, Mutation Analysis of the ASPM Gene in 18 Pakistani Families With Autosomal Recessive Primary Microcephaly, 10.1177/0883073809346850
  27. Kumar A, Blanton SH, Babu M, Markandaya M, Girimaji SC, Genetic analysis of primary microcephaly in Indian families: novel ASPM mutations : Primary microcephaly in Indian patients, 10.1111/j.1399-0004.2004.00304.x
  28. Marchal Juan Alberto, Ghani Mahdi, Schindler Detlev, Gavvovidis Ioannis, Winkler Tina, Esquitino Veronique, Sternberg Nadine, Busche Andreas, Krawitz Peter, Hecht Joachim, Robinson Peter, Mundlos Stephan, Graul-Neumann Luitgard, Sperling Karl, Trimborn Marc, Neitzel Heidemarie, Misregulation of mitotic chromosome segregation in a new type of autosomal recessive primary microcephaly, 10.4161/cc.10.17.16871
  29. Morris Joan K, Rankin Judith, Garne Ester, Loane Maria, Greenlees Ruth, Addor Marie-Claude, Arriola Larraitz, Barisic Ingeborg, Bergman Jorieke E H, Csaky-Szunyogh Melinda, Dias Carlos, Draper Elizabeth S, Gatt Miriam, Khoshnood Babak, Klungsoyr Kari, Kurinczuk Jennifer J, Lynch Catherine, McDonnell Robert, Nelen Vera, Neville Amanda J, O’Mahony Mary T, Pierini Anna, Randrianaivo Hanitra, Rissmann Anke, Tucker David, Verellen-Dumoulin Christine, de Walle Hermien E K, Wellesley Diana, Wiesel Awi, Dolk Helen, Prevalence of microcephaly in Europe: population based study, 10.1136/bmj.i4721
  30. Muhammad Farooq, Mahmood Baig Shahid, Hansen Lars, Sajid Hussain Muhammad, Anjum Inayat Iram, Aslam Muhammad, Anver Qureshi Javed, Toilat Muhammad, Kirst Elisabeth, Wajid Muhammad, Nürnberg Peter, Eiberg Hans, Tommerup Niels, Kjaer Klaus W., Compound heterozygous ASPM mutations in Pakistani MCPH families, 10.1002/ajmg.a.32749
  31. Nakamura Kazuyuki, Inui Takehiko, Miya Fuyuki, Kanemura Yonehiro, Okamoto Nobuhiko, Saitoh Shinji, Yamasaki Mami, Tsunoda Tatsuhiko, Kosaki Kenjiro, Tanaka Soichiro, Kato Mitsuhiro, Primary Microcephaly With Anterior Predominant Pachygyria Caused by Novel Compound Heterozygous Mutations in ASPM, 10.1016/j.pediatrneurol.2015.01.019
  32. Nicholas A K, Swanson E A, Cox J J, Karbani G, Malik S, Springell K, Hampshire D, Ahmed M, Bond J, Di Benedetto D, Fichera M, Romano C, Dobyns W B, Woods C G, The molecular landscape of ASPM mutations in primary microcephaly, 10.1136/jmg.2008.062380
  33. Papari E, Bastami M, Farhadi A, Abedini SS, Hosseini M, Bahman I, Mohseni M, Garshasbi M, Moheb L Abbasi, Behjati F, Kahrizi K, Ropers H-H, Najmabadi H, Investigation of primary microcephaly in Bushehr province of Iran: novelSTILand ASPMmutations : Letter to the Editor, 10.1111/j.1399-0004.2012.01949.x
  34. Paramasivam Murugan, Chang YoonJeung, LoTurco Joseph J., ASPM and Citron Kinase Co-Localize to the Midbody Ring during Cytokinesis, 10.4161/cc.6.13.4356
  35. Passemard, GeneReviews at GeneTests. Medical Genetics Information Resource, 1997 (2009a)
  36. Passemard S., Titomanlio L., Elmaleh M., Afenjar A., Alessandri J. -L., Andria G., de Villemeur T. B., Boespflug-Tanguy O., Burglen L., Del Giudice E., Guimiot F., Hyon C., Isidor B., Megarbane A., Moog U., Odent S., Hernandez K., Pouvreau N., Scala I., Schaer M., Gressens P., Gerard B., Verloes A., Expanding the clinical and neuroradiologic phenotype of primary microcephaly due to ASPM mutations, 10.1212/wnl.0b013e3181b8799a
  37. Passemard Sandrine, Verloes Alain, Billette de Villemeur Thierry, Boespflug-Tanguy Odile, Hernandez Karen, Laurent Marion, Isidor Bertrand, Alberti Corinne, Pouvreau Nathalie, Drunat Séverine, Gérard Bénédicte, El Ghouzzi Vincent, Gallego Jorge, Elmaleh-Bergès Monique, Huttner Wieland B., Eliez Stephan, Gressens Pierre, Schaer Marie, Abnormal spindle-like microcephaly-associated (ASPM) mutations strongly disrupt neocortical structure but spare the hippocampus and long-term memory, 10.1016/j.cortex.2015.10.010
  38. Pattison Lisa, Crow Yanick J., Deeble V. Jayne, Jackson Andrew P., Jafri Hussain, Rashid Yasmin, Roberts Emma, Woods C. Geoffrey, A Fifth Locus for Primary Autosomal Recessive Microcephaly Maps to Chromosome 1q31, 10.1086/316910
  39. Pichon Bruno, Vankerckhove Sophie, Bourrouillou Georges, Duprez Laurence, Abramowicz Marc J, A translocation breakpoint disrupts the ASPM gene in a patient with primary microcephaly, 10.1038/sj.ejhg.5201169
  40. Ponting Chris, Jackson Andrew P, Evolution of primary microcephaly genes and the enlargement of primate brains, 10.1016/j.gde.2005.04.009
  41. Pulvers J. N., Bryk J., Fish J. L., Wilsch-Brauninger M., Arai Y., Schreier D., Naumann R., Helppi J., Habermann B., Vogt J., Nitsch R., Toth A., Enard W., Paabo S., Huttner W. B., Mutations in mouse Aspm (abnormal spindle-like microcephaly associated) cause not only microcephaly but also major defects in the germline, 10.1073/pnas.1010494107
  42. Rump Patrick, Jazayeri Omid, van Dijk-Bos Krista K., Johansson Lennart F., van Essen Anthonie J., Verheij Johanna B. G. M., Veenstra-Knol Hermine E., Redeker Egbert J. W., Mannens Marcel M. A. M., Swertz Morris A., Alizadeh Behrooz Z., van Ravenswaaij-Arts Conny M. A., Sinke Richard J., Sikkema-Raddatz Birgit, Whole-exome sequencing is a powerful approach for establishing the etiological diagnosis in patients with intellectual disability and microcephaly, 10.1186/s12920-016-0167-8
  43. Saadi Abdelkrim, Borck Guntram, Boddaert Nathalie, Chekkour Mohamed Chahine, Imessaoudene Belaïd, Munnich Arnold, Colleaux Laurence, Chaouch Malika, Compound heterozygous ASPM mutations associated with microcephaly and simplified cortical gyration in a consanguineous Algerian family, 10.1016/j.ejmg.2009.03.013
  44. Sajid Hussain M, Marriam Bakhtiar S, Farooq M, Anjum I, Janzen E, Reza Toliat M, Eiberg H, Kjaer KW, Tommerup N, Noegel AA, Nürnberg P, Baig SM, Hansen L, Genetic heterogeneity in Pakistani microcephaly families : Pakistani microcephaly mutations, 10.1111/j.1399-0004.2012.01932.x
  45. Schou Kenneth B, Morthorst Stine K, Christensen Søren T, Pedersen Lotte B, Identification of conserved, centrosome-targeting ASH domains in TRAPPII complex subunits and TRAPPC8, 10.1186/2046-2530-3-6
  46. Sempé M, Auxologie-méthodes et séquences (1979)
  47. Shen J, ASPM mutations identified in patients with primary microcephaly and seizures, 10.1136/jmg.2004.027706
  48. Stradal Theresia, Kranewitter Wolfgang, Winder Steven J, Gimona Mario, CH domains revisited, 10.1016/s0014-5793(98)00751-0
  49. Tan CA, del Gaudio D., Dempsey M.A., Arndt K., Botes S., Reeder A., Das S., Analysis ofASPMin an ethnically diverse cohort of 400 patient samples: perspectives of the molecular diagnostic laboratory : Analysis of ASPM in an ethnically diverse cohort of 400 patient samples, 10.1111/cge.12172
  50. Thornton Gemma K., Woods C. Geoffrey, Primary microcephaly: do all roads lead to Rome?, 10.1016/j.tig.2009.09.011
  51. BOSCH J., MICROCEPHALY IN THE NETHERLANDS: A CLINICAL AND GENETICAL STUDY, 10.1111/j.1469-1809.1958.tb01455.x
  52. Verloes, GeneReviews®, 1993 (2013)
  53. Wang Rongrong, Khan Amjad, Han Shirui, Zhang Xue, Molecular analysis of 23 Pakistani families with autosomal recessive primary microcephaly using targeted next-generation sequencing, 10.1038/jhg.2016.128
  54. Woods C. G., Parker A., Investigating microcephaly, 10.1136/archdischild-2012-302882
Bibliographic reference Létard, Pascaline ; Drunat, Séverine ; Vial, Yoann ; Duerinckx, Sarah ; Ernault, Anais ; et. al. Autosomal recessive primary microcephaly due to ASPM mutations: An update. In: Human Mutation, Vol. 39, no. 3, p. 319-332 (2018)
Permanent URL http://hdl.handle.net/2078.1/219857