. 2019 Aug; 35(10):754-767.
doi: 10.1016/j.tig.2019.07.004.

Ribosomopathies: Old Concepts, New Controversies

Katherine I Farley-Barnes 1 Lisa M Ogawa 1 Susan J Baserga 2 
  • PMID: 31376929
  •     136 References
  •     26 citations


Ribosomopathies are a diverse subset of diseases caused by reduced expression of, or mutations in, factors necessary for making ribosomes, the protein translation machinery in the cell. Despite the ubiquitous need for ribosomes in all cell types, ribosomopathies manifest with tissue-specific defects and sometimes increased cancer susceptibility, but few treatments target the underlying cause. By highlighting new research in the field, we review current hypotheses for the basis of this tissue specificity. Based on new work, we broaden our understanding of the role of ribosome biogenesis in diverse tissue types throughout embryonic development. We also pose the question of whether previously described human conditions such as aging can be at least partially attributed to defects in making ribosomes.

Keywords: aging; cancer; neurodegeneration; ribosome concentration hypothesis; ribosomopathy; specialized ribosome.

Ribosomopathies: There's strength in numbers.
Eric W Mills, Rachel Green.
Science, 2017 Nov 04; 358(6363). PMID: 29097519
Highly Cited. Review.
Ribosome dysfunction is an early event in Alzheimer's disease.
Qunxing Ding, William R Markesbery, +2 authors, Jeffrey N Keller.
J Neurosci, 2005 Oct 07; 25(40). PMID: 16207876    Free PMC article.
Highly Cited.
Classification of and risk factors for hematologic complications in a French national cohort of 102 patients with Shwachman-Diamond syndrome.
Jean Donadieu, Odile Fenneteau, +18 authors, Associated investigators of the French Severe Chronic Neutropenia Registry*.
Haematologica, 2012 Apr 12; 97(9). PMID: 22491737    Free PMC article.
Altered translation of GATA1 in Diamond-Blackfan anemia.
Leif S Ludwig, Hanna T Gazda, +10 authors, Vijay G Sankaran.
Nat Med, 2014 Jun 24; 20(7). PMID: 24952648    Free PMC article.
Highly Cited.
Mutations in the ribosomal protein gene RPL10 suggest a novel modulating disease mechanism for autism.
S M Klauck, B Felder, +8 authors, A Poustka.
Mol Psychiatry, 2006 Aug 31; 11(12). PMID: 16940977
On protein synthesis.
Symp Soc Exp Biol, 1958 Jan 01; 12. PMID: 13580867
Highly Cited.
Cancer in the National Cancer Institute inherited bone marrow failure syndrome cohort after fifteen years of follow-up.
Blanche P Alter, Neelam Giri, Sharon A Savage, Philip S Rosenberg.
Haematologica, 2017 Oct 21; 103(1). PMID: 29051281    Free PMC article.
Highly Cited.
Rps26 directs mRNA-specific translation by recognition of Kozak sequence elements.
Max B Ferretti, Homa Ghalei, +2 authors, Katrin Karbstein.
Nat Struct Mol Biol, 2017 Aug 02; 24(9). PMID: 28759050    Free PMC article.
Highly Cited.
The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of Pre-rRNA processing factors.
Lionel Tafforeau, Christiane Zorbas, +5 authors, Denis L J Lafontaine.
Mol Cell, 2013 Aug 27; 51(4). PMID: 23973377
Highly Cited.
Emerging roles of the neuronal nucleolus.
Michal Hetman, Maciej Pietrzak.
Trends Neurosci, 2012 Feb 07; 35(5). PMID: 22305768    Free PMC article.
The plurifunctional nucleolus.
T Pederson.
Nucleic Acids Res, 1998 Aug 15; 26(17). PMID: 9705492    Free PMC article.
Highly Cited. Review.
The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia.
N Draptchinskaia, P Gustavsson, +11 authors, N Dahl.
Nat Genet, 1999 Feb 13; 21(2). PMID: 9988267
Highly Cited.
A protein inventory of human ribosome biogenesis reveals an essential function of exportin 5 in 60S subunit export.
Thomas Wild, Peter Horvath, +7 authors, Ulrike Kutay.
PLoS Biol, 2010 Nov 05; 8(10). PMID: 21048991    Free PMC article.
Treacher Collins syndrome: a clinical and molecular study based on a large series of patients.
Marie Vincent, David Geneviève, +54 authors, Corinne Collet.
Genet Med, 2015 Mar 20; 18(1). PMID: 25790162
Variable clinical presentation of Shwachman-Diamond syndrome: update from the North American Shwachman-Diamond Syndrome Registry.
Kasiani C Myers, Audrey Anna Bolyard, +6 authors, Akiko Shimamura.
J Pediatr, 2014 Jan 07; 164(4). PMID: 24388329    Free PMC article.
Treacher Collins Syndrome: the genetics of a craniofacial disease.
Sameep Kadakia, Samuel N Helman, +2 authors, Yadranko Ducic.
Int J Pediatr Otorhinolaryngol, 2014 Apr 03; 78(6). PMID: 24690222
Untranslated regions of mRNAs.
Flavio Mignone, Carmela Gissi, Sabino Liuni, Graziano Pesole.
Genome Biol, 2002 Mar 19; 3(3). PMID: 11897027    Free PMC article.
Highly Cited. Review.
Mutations in genes encoding subunits of RNA polymerases I and III cause Treacher Collins syndrome.
Johannes G Dauwerse, Jill Dixon, +17 authors, Dagmar Wieczorek.
Nat Genet, 2010 Dec 07; 43(1). PMID: 21131976
Increased Prevalence of Congenital Heart Disease in Children With Diamond Blackfan Anemia Suggests Unrecognized Diamond Blackfan Anemia as a Cause of Congenital Heart Disease in the General Population: A Report of the Diamond Blackfan Anemia Registry.
Adrianna Vlachos, Diana S Osorio, +13 authors, Jeffrey M Lipton.
Circ Genom Precis Med, 2018 May 12; 11(5). PMID: 29748317    Free PMC article.
Labrune syndrome: A unique leukoencephalopathy.
Leena Pahuja, Elisheba Patras, +2 authors, Laxmi Khanna.
Ann Indian Acad Neurol, 2017 Mar 17; 20(1). PMID: 28298845    Free PMC article.
Transcriptome analysis reveals a ribosome constituents disorder involved in the RPL5 downregulated zebrafish model of Diamond-Blackfan anemia.
Yang Wan, Qian Zhang, +10 authors, Xiangdong Fang.
BMC Med Genomics, 2016 Mar 11; 9. PMID: 26961822    Free PMC article.
Lamin B2 Modulates Nucleolar Morphology, Dynamics, and Function.
Ayantika Sen Gupta, Kundan Sengupta.
Mol Cell Biol, 2017 Oct 11; 37(24). PMID: 28993479    Free PMC article.
Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte.
B A Peculis, J A Steitz.
Cell, 1993 Jun 18; 73(6). PMID: 8513505
Highly Cited.
Inverse size scaling of the nucleolus by a concentration-dependent phase transition.
Stephanie C Weber, Clifford P Brangwynne.
Curr Biol, 2015 Feb 24; 25(5). PMID: 25702583    Free PMC article.
Highly Cited.
Warsaw breakage syndrome, a cohesinopathy associated with mutations in the XPD helicase family member DDX11/ChlR1.
Petra van der Lelij, Krystyna H Chrzanowska, +6 authors, Johan P de Winter.
Am J Hum Genet, 2010 Feb 09; 86(2). PMID: 20137776    Free PMC article.
Identification and biochemical characterization of a novel mutation in DDX11 causing Warsaw breakage syndrome.
José-Mario Capo-Chichi, Sanjay Kumar Bharti, +10 authors, Zoha Kibar.
Hum Mutat, 2012 Oct 04; 34(1). PMID: 23033317    Free PMC article.
Prognostic Mutations in Myelodysplastic Syndrome after Stem-Cell Transplantation.
R Coleman Lindsley, Wael Saber, +14 authors, Benjamin L Ebert.
N Engl J Med, 2017 Feb 09; 376(6). PMID: 28177873    Free PMC article.
Highly Cited.
Role of the nucleolus in neurodegenerative diseases with particular reference to the retina: a review.
Paul I Sia, John Pm Wood, +3 authors, Robert J Casson.
Clin Exp Ophthalmol, 2015 Oct 02; 44(3). PMID: 26427048
RNA function. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration.
Ryuta Ishimura, Gabor Nagy, +7 authors, Susan L Ackerman.
Science, 2014 Jul 26; 345(6195). PMID: 25061210    Free PMC article.
Highly Cited.
Werner complex deficiency in cells disrupts the Nuclear Pore Complex and the distribution of lamin B1.
Zhi Li, Yizhou Zhu, +4 authors, Joseph S Glavy.
Biochim Biophys Acta, 2013 Sep 21; 1833(12). PMID: 24050918
Ribosome Stoichiometry: From Form to Function.
Edward Emmott, Marko Jovanovic, Nikolai Slavov.
Trends Biochem Sci, 2018 Nov 27; 44(2). PMID: 30473427    Free PMC article.
RNA synthesis and control of cell division in the yeast S. cerevisiae.
G C Johnston, R A Singer.
Cell, 1978 Aug 01; 14(4). PMID: 99247
Highly Cited.
Ribosomal DNA and cellular senescence: new evidence supporting the connection between rDNA and aging.
Austen R D Ganley, Takehiko Kobayashi.
FEMS Yeast Res, 2014 Jan 01; 14(1). PMID: 24373458
A Ribosomopathy Reveals Decoding Defective Ribosomes Driving Human Dysmorphism.
Nahuel A Paolini, Martin Attwood, +17 authors, Alyson W MacInnes.
Am J Hum Genet, 2017 Mar 05; 100(3). PMID: 28257692    Free PMC article.
Distinct haematological disorder with deletion of long arm of no. 5 chromosome.
H Van den Berghe, J J Cassiman, +3 authors, G Sokal.
Nature, 1974 Oct 04; 251(5474). PMID: 4421285
Highly Cited.
Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects.
Kelly A McGowan, Jun Z Li, +9 authors, Gregory S Barsh.
Nat Genet, 2008 Jul 22; 40(8). PMID: 18641651    Free PMC article.
Highly Cited.
Incomplete penetrance for isolated congenital asplenia in humans with mutations in translated and untranslated RPSA exons.
Alexandre Bolze, Bertrand Boisson, +37 authors, Jean-Laurent Casanova.
Proc Natl Acad Sci U S A, 2018 Aug 04; 115(34). PMID: 30072435    Free PMC article.
Ribosomal DNA copy number amplification and loss in human cancers is linked to tumor genetic context, nucleolus activity, and proliferation.
Meng Wang, Bernardo Lemos.
PLoS Genet, 2017 Sep 08; 13(9). PMID: 28880866    Free PMC article.
Highly Cited.
Impaired ribosome biogenesis: mechanisms and relevance to cancer and aging.
Zsofia Turi, Matthew Lacey, Martin Mistrik, Pavel Moudry.
Aging (Albany NY), 2019 Apr 27; 11(8). PMID: 31026227    Free PMC article.
Nucleolar expansion and elevated protein translation in premature aging.
Abigail Buchwalter, Martin W Hetzer.
Nat Commun, 2017 Sep 01; 8(1). PMID: 28855503    Free PMC article.
Highly Cited.
Ribosomal biogenesis genes play an essential and p53-independent role in zebrafish pancreas development.
Elayne Provost, Karen A Wehner, +5 authors, Steven D Leach.
Development, 2012 Aug 09; 139(17). PMID: 22872088    Free PMC article.
The sequence of the 5' end of the U8 small nucleolar RNA is critical for 5.8S and 28S rRNA maturation.
B A Peculis.
Mol Cell Biol, 1997 Jul 01; 17(7). PMID: 9199304    Free PMC article.
Gross deletions in TCOF1 are a cause of Treacher-Collins-Franceschetti syndrome.
Michael Bowman, Michael Oldridge, +5 authors, Tracy Lester.
Eur J Hum Genet, 2012 Feb 10; 20(7). PMID: 22317976    Free PMC article.
The C-terminus of Utp4, mutated in childhood cirrhosis, is essential for ribosome biogenesis.
Emily F Freed, Susan J Baserga.
Nucleic Acids Res, 2010 Apr 14; 38(14). PMID: 20385600    Free PMC article.
Cockayne syndrome: Clinical features, model systems and pathways.
Ajoy C Karikkineth, Morten Scheibye-Knudsen, +2 authors, Vilhelm A Bohr.
Ageing Res Rev, 2016 Oct 22; 33. PMID: 27507608    Free PMC article.
Highly Cited. Review.
Nucleolar disruption in dopaminergic neurons leads to oxidative damage and parkinsonism through repression of mammalian target of rapamycin signaling.
Claus Rieker, David Engblom, +8 authors, Rosanna Parlato.
J Neurosci, 2011 Jan 14; 31(2). PMID: 21228155    Free PMC article.
Transcriptome Profiling Identifies Ribosome Biogenesis as a Target of Alcohol Teratogenicity and Vulnerability during Early Embryogenesis.
Mark E Berres, Ana Garic, George R Flentke, Susan M Smith.
PLoS One, 2017 Jan 04; 12(1). PMID: 28046103    Free PMC article.
Fanconi anemia protein FANCI functions in ribosome biogenesis.
Samuel B Sondalle, Simonne Longerich, +2 authors, Susan J Baserga.
Proc Natl Acad Sci U S A, 2019 Jan 30; 116(7). PMID: 30692263    Free PMC article.
A brother and sister with intellectual disability and characteristic neuroimaging findings.
Marjolein Hermens, Marjo S van der Knaap, Erik-Jan Kamsteeg, Michèl A Willemsen.
Eur J Paediatr Neurol, 2018 Jul 05; 22(5). PMID: 29970281
Altered Machinery of Protein Synthesis in Alzheimer's: From the Nucleolus to the Ribosome.
Karina Hernández-Ortega, Paula Garcia-Esparcia, +2 authors, Isidre Ferrer.
Brain Pathol, 2015 Oct 30; 26(5). PMID: 26512942
A novel ribosomopathy caused by dysfunction of RPL10 disrupts neurodevelopment and causes X-linked microcephaly in humans.
Susan S Brooks, Alissa L Wall, +7 authors, Erica E Davis.
Genetics, 2014 Oct 16; 198(2). PMID: 25316788    Free PMC article.
Mutation in ribosomal protein L21 underlies hereditary hypotrichosis simplex.
Cheng Zhou, Dongjie Zang, +4 authors, Jianzhong Zhang.
Hum Mutat, 2011 Mar 18; 32(7). PMID: 21412954
Extrachromosomal rDNA circles--a cause of aging in yeast.
D A Sinclair, L Guarente.
Cell, 1998 Jan 15; 91(7). PMID: 9428525
Highly Cited.
The Treacher Collins syndrome (TCOF1) gene product is involved in pre-rRNA methylation.
Bianca Gonzales, Dale Henning, +3 authors, Benigno C Valdez.
Hum Mol Genet, 2005 Jun 03; 14(14). PMID: 15930015
Deletion of chromosome 20 in bone marrow of patients with Shwachman-Diamond syndrome, loss of the EIF6 gene and benign prognosis.
Barbara Pressato, Roberto Valli, +5 authors, Emanuela Maserati.
Br J Haematol, 2012 Feb 03; 157(4). PMID: 22295858
Diamond-Blackfan anemia with mandibulofacial dystostosis is heterogeneous, including the novel DBA genes TSR2 and RPS28.
Karen W Gripp, Cynthia Curry, +8 authors, Katia Sol-Church.
Am J Med Genet A, 2014 Jun 20; 164A(9). PMID: 24942156    Free PMC article.
The Roles of RNA Polymerase I and III Subunits Polr1c and Polr1d in Craniofacial Development and in Zebrafish Models of Treacher Collins Syndrome.
Kristin E Noack Watt, Annita Achilleos, +2 authors, Paul A Trainor.
PLoS Genet, 2016 Jul 23; 12(7). PMID: 27448281    Free PMC article.
Molecular basis of the human ribosomopathy Shwachman-Diamond syndrome.
Alan J Warren.
Adv Biol Regul, 2017 Sep 25; 67. PMID: 28942353    Free PMC article.
PAK1IP1, a ribosomal stress-induced nucleolar protein, regulates cell proliferation via the p53-MDM2 loop.
Weishi Yu, Zhongwei Qiu, +9 authors, Mingyao Liu.
Nucleic Acids Res, 2010 Nov 26; 39(6). PMID: 21097889    Free PMC article.
Ribosomopathies: how a common root can cause a tree of pathologies.
Nadia Danilova, Hanna T Gazda.
Dis Model Mech, 2015 Sep 24; 8(9). PMID: 26398160    Free PMC article.
Highly Cited. Review.
Dyskeratosis congenita in all its forms.
I Dokal.
Br J Haematol, 2000 Oct 29; 110(4). PMID: 11054058
Highly Cited. Review.
Ear malformations, hearing loss and hearing rehabilitation in children with Treacher Collins syndrome.
Francisco Rosa, Miguel Bebiano Coutinho, João Pinto Ferreira, Cecilia Almeida Sousa.
Acta Otorrinolaringol Esp, 2015 May 31; 67(3). PMID: 26025357
Tissue specific roles for the ribosome biogenesis factor Wdr43 in zebrafish development.
Chengtian Zhao, Viktoria Andreeva, +8 authors, Pamela C Yelick.
PLoS Genet, 2014 Feb 06; 10(1). PMID: 24497835    Free PMC article.
High mutation detection rate in TCOF1 among Treacher Collins syndrome patients reveals clustering of mutations and 16 novel pathogenic changes.
A Splendore, E O Silva, +7 authors, M R Passos-Bueno.
Hum Mutat, 2000 Oct 03; 16(4). PMID: 11013442
The ribosome biogenesis protein Esf1 is essential for pharyngeal cartilage formation in zebrafish.
Jian-Yang Chen, Xungang Tan, +5 authors, Yun Li.
FEBS J, 2018 Aug 04; 285(18). PMID: 30073783
A de novo mutation in RPL10 causes a rare X-linked ribosomopathy characterized by syndromic intellectual disability and epilepsy: A new case and review of the literature.
Danielle K Bourque, Taila Hartley, +5 authors, David A Dyment.
Eur J Med Genet, 2017 Oct 27; 61(2). PMID: 29066376
Novel recurrent chromosome anomalies in Shwachman-Diamond syndrome.
Roberto Valli, Elena De Paoli, +3 authors, Emanuela Maserati.
Pediatr Blood Cancer, 2017 Jan 29; 64(8). PMID: 28130858
Dysregulation of RNA polymerase I transcription during disease.
K M Hannan, E Sanij, +2 authors, R B Pearson.
Biochim Biophys Acta, 2012 Nov 17; 1829(3-4). PMID: 23153826    Free PMC article.
Cytogenetic monitoring in Shwachman-Diamond syndrome: a note on clonal progression and a practical warning.
Barbara Pressato, Roberto Valli, +5 authors, Emanuela Maserati.
J Pediatr Hematol Oncol, 2015 Apr 19; 37(4). PMID: 25887640
Use of the iNo score to discriminate normal from altered nucleolar morphology, with applications in basic cell biology and potential in human disease diagnostics.
Vassiliki Stamatopoulou, Pascaline Parisot, Christophe De Vleeschouwer, Denis L J Lafontaine.
Nat Protoc, 2018 Sep 27; 13(10). PMID: 30250292
Genome-wide RNAi Screening Identifies Protein Modules Required for 40S Subunit Synthesis in Human Cells.
Lukas Badertscher, Thomas Wild, +10 authors, Ulrike Kutay.
Cell Rep, 2015 Dec 30; 13(12). PMID: 26711351
Rare ribosomopathies: insights into mechanisms of cancer.
Anna Aspesi, Steven R Ellis.
Nat Rev Cancer, 2019 Jan 24; 19(4). PMID: 30670820
Highly Cited. Review.
Mutations in SBDS are associated with Shwachman-Diamond syndrome.
Graeme R B Boocock, Jodi A Morrison, +4 authors, Johanna M Rommens.
Nat Genet, 2002 Dec 24; 33(1). PMID: 12496757
Highly Cited.
Nucleolar stress with and without p53.
Allison James, Yubo Wang, +2 authors, Patrick DiMario.
Nucleus, 2014 Dec 09; 5(5). PMID: 25482194    Free PMC article.
Highly Cited. Review.
Mutation and expression analyses of the ribosomal protein gene RPL10 in an extended German sample of patients with autism spectrum disorder.
A Chiocchetti, G Pakalapati, +4 authors, S M Klauck.
Am J Med Genet A, 2011 May 14; 155A(6). PMID: 21567917
The ribosome biogenesis factor Nol11 is required for optimal rDNA transcription and craniofacial development in Xenopus.
John N Griffin, Samuel B Sondalle, +2 authors, Mustafa K Khokha.
PLoS Genet, 2015 Mar 11; 11(3). PMID: 25756904    Free PMC article.
Exome sequencing identifies mutation in CNOT3 and ribosomal genes RPL5 and RPL10 in T-cell acute lymphoblastic leukemia.
Kim De Keersmaecker, Zeynep Kalender Atak, +27 authors, Jan Cools.
Nat Genet, 2012 Dec 25; 45(2). PMID: 23263491    Free PMC article.
Highly Cited.
Mutations in SNORD118 cause the cerebral microangiopathy leukoencephalopathy with calcifications and cysts.
Emma M Jenkinson, Mathieu P Rodero, +63 authors, Yanick J Crow.
Nat Genet, 2016 Aug 30; 48(10). PMID: 27571260    Free PMC article.
How common are extraribosomal functions of ribosomal proteins?
Jonathan R Warner, Kerri B McIntosh.
Mol Cell, 2009 Apr 14; 34(1). PMID: 19362532    Free PMC article.
Highly Cited. Review.
Acrofacial Dysostosis, Cincinnati Type, a Mandibulofacial Dysostosis Syndrome with Limb Anomalies, Is Caused by POLR1A Dysfunction.
K Nicole Weaver, Kristin E Noack Watt, +12 authors, Howard M Saal.
Am J Hum Genet, 2015 Apr 29; 96(5). PMID: 25913037    Free PMC article.
Proteasomal inhibition attenuates craniofacial malformations in a zebrafish model of Treacher Collins Syndrome.
Mauco Gil Rosas, Agustín Lorenzatti, +2 authors, Gabriela Coux.
Biochem Pharmacol, 2019 Mar 09; 163. PMID: 30849304
Diverse Regulators of Human Ribosome Biogenesis Discovered by Changes in Nucleolar Number.
Katherine I Farley-Barnes, Kathleen L McCann, +3 authors, Susan J Baserga.
Cell Rep, 2018 Feb 15; 22(7). PMID: 29444442    Free PMC article.
Highly Cited.
Cancer Biogenesis in Ribosomopathies.
Sergey O Sulima, Kim R Kampen, Kim De Keersmaecker.
Cells, 2019 Mar 14; 8(3). PMID: 30862070    Free PMC article.
Prevalence of dental anomalies, ectopic eruption and associated oral malformations in subjects with Treacher Collins syndrome.
Gisele da Silva Dalben, Beatriz Costa, Marcia Ribeiro Gomide.
Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 2006 Apr 25; 101(5). PMID: 16632269
A mutation in mouse Pak1ip1 causes orofacial clefting while human PAK1IP1 maps to 6p24 translocation breaking points associated with orofacial clefting.
Adam P Ross, M Adela Mansilla, +12 authors, Konstantinos S Zarbalis.
PLoS One, 2013 Aug 13; 8(7). PMID: 23935987    Free PMC article.
DNAJC21 Mutations Link a Cancer-Prone Bone Marrow Failure Syndrome to Corruption in 60S Ribosome Subunit Maturation.
Hemanth Tummala, Amanda J Walne, +13 authors, Tom Vulliamy.
Am J Hum Genet, 2016 Jun 28; 99(1). PMID: 27346687    Free PMC article.
Mesenchymal Inflammation Drives Genotoxic Stress in Hematopoietic Stem Cells and Predicts Disease Evolution in Human Pre-leukemia.
Noemi A Zambetti, Zhen Ping, +20 authors, Marc H G P Raaijmakers.
Cell Stem Cell, 2016 Sep 27; 19(5). PMID: 27666011
Highly Cited.
Refining the phenotype associated with biallelic DNAJC21 mutations.
G D'Amours, F Lopes, +12 authors, J-F Soucy.
Clin Genet, 2018 Apr 28; 94(2). PMID: 29700810
Analysis of clinical and immunologic phenotype in a large cohort of children and adults with cartilage-hair hypoplasia.
Svetlana Kostjukovits, Paula Klemetti, +5 authors, Outi Mäkitie.
J Allergy Clin Immunol, 2017 Mar 13; 140(2). PMID: 28284971    Free PMC article.
Dissecting the transcriptional phenotype of ribosomal protein deficiency: implications for Diamond-Blackfan Anemia.
Anna Aspesi, Elisa Pavesi, +16 authors, Irma Dianzani.
Gene, 2014 May 20; 545(2). PMID: 24835311    Free PMC article.
Small nucleoli are a cellular hallmark of longevity.
Varnesh Tiku, Chirag Jain, +9 authors, Adam Antebi.
Nat Commun, 2017 Aug 31; 8. PMID: 28853436    Free PMC article.
Highly Cited.
The Treacher Collins syndrome (TCOF1) gene product is involved in ribosomal DNA gene transcription by interacting with upstream binding factor.
Benigno C Valdez, Dale Henning, +2 authors, Michael J Dixon.
Proc Natl Acad Sci U S A, 2004 Jul 14; 101(29). PMID: 15249688    Free PMC article.
Ribosomal protein SA haploinsufficiency in humans with isolated congenital asplenia.
Alexandre Bolze, Nizar Mahlaoui, +29 authors, Jean-Laurent Casanova.
Science, 2013 Apr 13; 340(6135). PMID: 23579497    Free PMC article.
Highly Cited.
Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning.
Nadya Kondrashov, Aya Pusic, +5 authors, Maria Barna.
Cell, 2011 May 03; 145(3). PMID: 21529712    Free PMC article.
Highly Cited.
Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function.
Natalie C Jones, Megan L Lynn, +9 authors, Paul A Trainor.
Nat Med, 2008 Feb 05; 14(2). PMID: 18246078    Free PMC article.
Highly Cited.
How Parkinson's disease meets nucleolar stress.
Rosanna Parlato, Birgit Liss.
Biochim Biophys Acta, 2014 Jan 15; 1842(6). PMID: 24412806
Shwachman-Diamond syndrome with clonal interstitial deletion of the long arm of chromosome 20 in bone marrow: haematological features, prognosis and genomic instability.
Roberto Valli, Antonella Minelli, +13 authors, Emanuela Maserati.
Br J Haematol, 2018 Dec 27; 184(6). PMID: 30585299
Widespread Accumulation of Ribosome-Associated Isolated 3' UTRs in Neuronal Cell Populations of the Aging Brain.
Peter H Sudmant, Hyeseung Lee, +2 authors, Christopher B Burge.
Cell Rep, 2018 Nov 30; 25(9). PMID: 30485811    Free PMC article.
Link between aging and the nucleolus.
L Guarente.
Genes Dev, 1997 Oct 23; 11(19). PMID: 9334311
Nucleolar activity in neurodegenerative diseases: a missing piece of the puzzle?
Rosanna Parlato, Grzegorz Kreiner.
J Mol Med (Berl), 2012 Nov 28; 91(5). PMID: 23179684    Free PMC article.
In Vivo Senescence in the Sbds-Deficient Murine Pancreas: Cell-Type Specific Consequences of Translation Insufficiency.
Marina E Tourlakis, Siyi Zhang, +7 authors, Johanna M Rommens.
PLoS Genet, 2015 Jun 10; 11(6). PMID: 26057580    Free PMC article.
Leukoencephalopathy, Intracranial Calcifications, Cysts, and SNORD118 Mutation (Labrune Syndrome) with Obstructive Hydrocephalus.
Anan Shtaya, Frances Elmslie, Yanick Crow, Samantha Hettige.
World Neurosurg, 2019 Feb 23; 125. PMID: 30794980
Evaluation and Management of Hematopoietic Failure in Dyskeratosis Congenita.
Suneet Agarwal.
Hematol Oncol Clin North Am, 2018 Jul 27; 32(4). PMID: 30047419    Free PMC article.
The mesenchymal niche in MDS.
Eline Pronk, Marc H G P Raaijmakers.
Blood, 2019 Jan 24; 133(10). PMID: 30670448
RNA regulons in Hox 5' UTRs confer ribosome specificity to gene regulation.
Shifeng Xue, Siqi Tian, +3 authors, Maria Barna.
Nature, 2014 Nov 20; 517(7532). PMID: 25409156    Free PMC article.
Highly Cited.
tp53-dependent and independent signaling underlies the pathogenesis and possible prevention of Acrofacial Dysostosis-Cincinnati type.
Kristin E N Watt, Cynthia L Neben, +2 authors, Paul A Trainor.
Hum Mol Genet, 2018 May 12; 27(15). PMID: 29750247    Free PMC article.
Genotyping in 46 patients with tentative diagnosis of Treacher Collins syndrome revealed unexpected phenotypic variation.
Ozge Altug Teber, Gabriele Gillessen-Kaesbach, +22 authors, Dagmar Wieczorek.
Eur J Hum Genet, 2004 Sep 02; 12(11). PMID: 15340364
mTORC Inhibitors as Broad-Spectrum Therapeutics for Age-Related Diseases.
Hannah E Walters, Lynne S Cox.
Int J Mol Sci, 2018 Aug 12; 19(8). PMID: 30096787    Free PMC article.
BMS1 is mutated in aplasia cutis congenita.
Alexander G Marneros.
PLoS Genet, 2013 Jun 21; 9(6). PMID: 23785305    Free PMC article.
The Warsaw breakage syndrome-related protein DDX11 is required for ribosomal RNA synthesis and embryonic development.
Xinliang Sun, Hongbo Chen, +6 authors, Lan Ma.
Hum Mol Genet, 2015 Jun 20; 24(17). PMID: 26089203
Alopecia, neurological defects, and endocrinopathy syndrome caused by decreased expression of RBM28, a nucleolar protein associated with ribosome biogenesis.
Janna Nousbeck, Ronen Spiegel, +13 authors, Eli Sprecher.
Am J Hum Genet, 2008 Apr 29; 82(5). PMID: 18439547    Free PMC article.
Nucleolar Function in Lifespan Regulation.
Varnesh Tiku, Adam Antebi.
Trends Cell Biol, 2018 May 22; 28(8). PMID: 29779866
Model for the regulation of mRNA translation applied to haemoglobin synthesis.
H F Lodish.
Nature, 1974 Oct 04; 251(5474). PMID: 4421673
Highly Cited.
Heterogeneous Ribosomes Preferentially Translate Distinct Subpools of mRNAs Genome-wide.
Zhen Shi, Kotaro Fujii, +4 authors, Maria Barna.
Mol Cell, 2017 Jun 20; 67(1). PMID: 28625553    Free PMC article.
Highly Cited.
Recessive TAF1A mutations reveal ribosomopathy in siblings with end-stage pediatric dilated cardiomyopathy.
Pamela A Long, Jeanne L Theis, +5 authors, Timothy M Olson.
Hum Mol Genet, 2017 May 05; 26(15). PMID: 28472305    Free PMC article.
Improving clinical care and elucidating the pathophysiology of Diamond Blackfan anemia: an update from the Diamond Blackfan Anemia Registry.
Jeffrey M Lipton, Eva Atsidaftos, Israel Zyskind, Adrianna Vlachos.
Pediatr Blood Cancer, 2005 Dec 01; 46(5). PMID: 16317735
Classical inherited bone marrow failure syndromes with high risk for myelodysplastic syndrome and acute myelogenous leukemia.
Sharon A Savage, Carlo Dufour.
Semin Hematol, 2017 Jun 24; 54(2). PMID: 28637614
Does functional specialization of ribosomes really exist?
Max B Ferretti, Katrin Karbstein.
RNA, 2019 Feb 09; 25(5). PMID: 30733326    Free PMC article.
Highly Cited. Review.
Different loss of material in recurrent chromosome 20 interstitial deletions in Shwachman-Diamond syndrome and in myeloid neoplasms.
Roberto Valli, Barbara Pressato, +5 authors, Emanuela Maserati.
Mol Cytogenet, 2013 Dec 18; 6(1). PMID: 24330778    Free PMC article.
The Discovery of Ribosome Heterogeneity and Its Implications for Gene Regulation and Organismal Life.
Naomi R Genuth, Maria Barna.
Mol Cell, 2018 Aug 04; 71(3). PMID: 30075139    Free PMC article.
Highly Cited. Review.
Riddle: what do aplastic anemia, paroxysmal nocturnal hemoglobinuria (PNH) and "hypoplastic" leukemia have in common?
W Dameshek.
Blood, 1967 Aug 01; 30(2). PMID: 6031145
RPSA, a candidate gene for isolated congenital asplenia, is required for pre-rRNA processing and spleen formation in Xenopus.
John N Griffin, Samuel B Sondalle, +6 authors, Mustafa K Khokha.
Development, 2018 Oct 20; 145(20). PMID: 30337486    Free PMC article.
Ribosome biogenesis in the yeast Saccharomyces cerevisiae.
John L Woolford, Susan J Baserga.
Genetics, 2013 Nov 06; 195(3). PMID: 24190922    Free PMC article.
Highly Cited. Review.
Mechanism of eIF6 release from the nascent 60S ribosomal subunit.
Félix Weis, Emmanuel Giudice, +6 authors, Alan J Warren.
Nat Struct Mol Biol, 2015 Oct 20; 22(11). PMID: 26479198    Free PMC article.
Highly Cited.
J Pediatr, 1964 Nov 01; 65. PMID: 14221166
Highly Cited.
Clinical features of dyskeratosis congenita in mainland China: case reports and literature review.
Fuxing Li, Wei Li, Xiaohong Qiao, Xiaotian Xie.
Int J Hematol, 2019 Jan 04; 109(3). PMID: 30604317
Ribosome Levels Selectively Regulate Translation and Lineage Commitment in Human Hematopoiesis.
Rajiv K Khajuria, Mathias Munschauer, +24 authors, Vijay G Sankaran.
Cell, 2018 Mar 20; 173(1). PMID: 29551269    Free PMC article.
Highly Cited.
An overview of pre-ribosomal RNA processing in eukaryotes.
Anthony K Henras, Célia Plisson-Chastang, +2 authors, Pierre-Emmanuel Gleizes.
Wiley Interdiscip Rev RNA, 2014 Oct 28; 6(2). PMID: 25346433    Free PMC article.
Highly Cited. Review.
Heterozygous De Novo UBTF Gain-of-Function Variant Is Associated with Neurodegeneration in Childhood.
Simon Edvardson, Claudia M Nicolae, +14 authors, Orly Elpeleg.
Am J Hum Genet, 2017 Aug 05; 101(2). PMID: 28777933    Free PMC article.
Longitudinal clinical and neuro-radiological findings in a patient with leukoencephalopathy with brain calcifications and cysts (Labrune syndrome).
Yasushi Iwasaki, Ken-Ichiro Hoshino, +6 authors, Mari Yoshida.
eNeurologicalSci, 2017 Dec 21; 8. PMID: 29260032    Free PMC article.
Telomerase reverse-transcriptase homozygous mutations in autosomal recessive dyskeratosis congenita and Hoyeraal-Hreidarsson syndrome.
Anna Marrone, Amanda Walne, +5 authors, Inderjeet Dokal.
Blood, 2007 Sep 06; 110(13). PMID: 17785587    Free PMC article.
C9orf72-associated neurodegeneration in ALS-FTD: breaking new ground in ribosomal RNA and nucleolar dysfunction.
Dustin Herrmann, Rosanna Parlato.
Cell Tissue Res, 2018 Feb 17; 373(2). PMID: 29450726
Tissue-selective effects of nucleolar stress and rDNA damage in developmental disorders.
Eliezer Calo, Bo Gu, +8 authors, Joanna Wysocka.
Nature, 2018 Jan 25; 554(7690). PMID: 29364875    Free PMC article.
Highly Cited.
Small and Large Ribosomal Subunit Deficiencies Lead to Distinct Gene Expression Signatures that Reflect Cellular Growth Rate.
Ze Cheng, Christopher Frederick Mugler, +7 authors, Gloria Ann Brar.
Mol Cell, 2018 Dec 07; 73(1). PMID: 30503772    Free PMC article.
A missense mutation (R565W) in cirhin (FLJ14728) in North American Indian childhood cirrhosis.
Pierre Chagnon, Jacques Michaud, +6 authors, Andrea Richter.
Am J Hum Genet, 2002 Nov 06; 71(6). PMID: 12417987    Free PMC article.
A case report on a rare disease: dyskeratosis congenita.
Bethel Shiferaw, Satish Mukka, +2 authors, Radhames Ramos De Oleo.
J Clin Med Res, 2015 Mar 18; 7(5). PMID: 25780486    Free PMC article.
Shaping the Nascent Ribosome: AAA-ATPases in Eukaryotic Ribosome Biogenesis.
Michael Prattes, Yu-Hua Lo, Helmut Bergler, Robin E Stanley.
Biomolecules, 2019 Nov 11; 9(11). PMID: 31703473    Free PMC article.
The Role of RNA Binding Proteins for Local mRNA Translation: Implications in Neurological Disorders.
Maximilian Paul Thelen, Min Jeong Kye.
Front Mol Biosci, 2020 Feb 06; 6. PMID: 32010708    Free PMC article.
Nucleolar Organization and Functions in Health and Disease.
Ursula Stochaj, Stephanie C Weber.
Cells, 2020 Feb 29; 9(3). PMID: 32106410    Free PMC article.
Fluoride exposure alters Ca2+ signaling and mitochondrial function in enamel cells.
Francisco J Aulestia, Johnny Groeling, +9 authors, Rodrigo S Lacruz.
Sci Signal, 2020 Feb 20; 13(619). PMID: 32071168    Free PMC article.
From Snapshots to Flipbook-Resolving the Dynamics of Ribosome Biogenesis with Chemical Probes.
Lisa Kofler, Michael Prattes, Helmut Bergler.
Int J Mol Sci, 2020 Apr 29; 21(8). PMID: 32340379    Free PMC article.
Myc as a Regulator of Ribosome Biogenesis and Cell Competition: A Link to Cancer.
Francesca Destefanis, Valeria Manara, Paola Bellosta.
Int J Mol Sci, 2020 Jun 11; 21(11). PMID: 32516899    Free PMC article.
Translatome Analyses Using Conditional Ribosomal Tagging in GABAergic Interneurons and Other Sparse Cell Types.
Vivek Mahadevan, Areg Peltekian, Chris J McBain.
Curr Protoc Neurosci, 2020 Jun 26; 92(1). PMID: 32584517    Free PMC article.
A memory of eS25 loss drives resistance phenotypes.
Alex G Johnson, Ryan A Flynn, +9 authors, Joseph D Puglisi.
Nucleic Acids Res, 2020 May 29; 48(13). PMID: 32463448    Free PMC article.
Paired Box 9 (PAX9), the RNA polymerase II transcription factor, regulates human ribosome biogenesis and craniofacial development.
Katherine I Farley-Barnes, Engin Deniz, +2 authors, Susan J Baserga.
PLoS Genet, 2020 Aug 20; 16(8). PMID: 32813698    Free PMC article.
The Existence and Localization of Nuclear snoRNAs in Arabidopsis thaliana Revisited.
Deniz Streit, Thiruvenkadam Shanmugam, +2 authors, Enrico Schleiff.
Plants (Basel), 2020 Aug 19; 9(8). PMID: 32806552    Free PMC article.
Recent advances in the nucleolar responses to DNA double-strand breaks.
Lea Milling Korsholm, Zita Gál, +4 authors, Dorthe Helena Larsen.
Nucleic Acids Res, 2020 Aug 29; 48(17). PMID: 32857853    Free PMC article.
Homeostatic Roles of the Proteostasis Network in Dendrites.
Erin N Lottes, Daniel N Cox.
Front Cell Neurosci, 2020 Oct 06; 14. PMID: 33013325    Free PMC article.
An Alternative Splicing Program for Mouse Craniofacial Development.
Joan E Hooper, Kenneth L Jones, +2 authors, Hong Li.
Front Physiol, 2020 Oct 06; 11. PMID: 33013468    Free PMC article.
Ribosomopathies: New Therapeutic Perspectives.
Emilien Orgebin, François Lamoureux, +4 authors, Marc Baud'huin.
Cells, 2020 Sep 17; 9(9). PMID: 32932838    Free PMC article.
Structural Heterogeneities of the Ribosome: New Frontiers and Opportunities for Cryo-EM.
Frédéric Poitevin, Artem Kushner, Xinpei Li, Khanh Dao Duc.
Molecules, 2020 Sep 23; 25(18). PMID: 32957592    Free PMC article.
Diphthamide-deficiency syndrome: a novel human developmental disorder and ribosomopathy.
Harmen Hawer, Bryce A Mendelsohn, +6 authors, Raffael Schaffrath.
Eur J Hum Genet, 2020 Jun 25; 28(11). PMID: 32576952    Free PMC article.
How Altered Ribosome Production Can Cause or Contribute to Human Disease: The Spectrum of Ribosomopathies.
Giulia Venturi, Lorenzo Montanaro.
Cells, 2020 Oct 21; 9(10). PMID: 33076379    Free PMC article.
The chemotherapeutic agent CX-5461 irreversibly blocks RNA polymerase I initiation and promoter release to cause nucleolar disruption, DNA damage and cell inviability.
Jean-Clément Mars, Michel G Tremblay, +4 authors, Tom Moss.
NAR Cancer, 2020 Nov 17; 2(4). PMID: 33196044    Free PMC article.
Ribosomal Protein L10: From Function to Dysfunction.
Daniela Pollutri, Marianna Penzo.
Cells, 2020 Nov 25; 9(11). PMID: 33227977    Free PMC article.
Ribosomopathy-associated mutations cause proteotoxic stress that is alleviated by TOR inhibition.
Carles Recasens-Alvarez, Cyrille Alexandre, +4 authors, Jean-Paul Vincent.
Nat Cell Biol, 2021 Jan 27; 23(2). PMID: 33495632    Free PMC article.
The nucleolus as a multiphase liquid condensate.
Denis L J Lafontaine, Joshua A Riback, Rümeyza Bascetin, Clifford P Brangwynne.
Nat Rev Mol Cell Biol, 2020 Sep 03; 22(3). PMID: 32873929
Tissue-Specific Ribosome Profiling in Drosophila.
Xun Chen, Dion Dickman.
Methods Mol Biol, 2021 Mar 26; 2252. PMID: 33765275
Structural overview of macromolecular machines involved in ribosome biogenesis.
Meredith N Frazier, Monica C Pillon, +2 authors, Robin E Stanley.
Curr Opin Struct Biol, 2020 Oct 26; 67. PMID: 33099228    Free PMC article.
Increased numbers of nucleoli in a genome-wide RNAi screen reveal proteins that link the cell cycle to RNA polymerase I transcription.
Lisa M Ogawa, Amber F Buhagiar, +3 authors, Susan J Baserga.
Mol Biol Cell, 2021 Mar 11; 32(9). PMID: 33689394    Free PMC article.
Paediatric neurosurgical implications of a ribosomopathy: illustrative case and literature review.
Suzanne Murphy, Gabriella Grima, Kshitij Mankad, Kristian Aquilina.
Childs Nerv Syst, 2021 May 22;. PMID: 34018027
Biallelic splicing variants in the nucleolar 60S assembly factor RBM28 cause the ribosomopathy ANE syndrome.
Carson J Bryant, Cláudia F Lorea, +4 authors, Susan J Baserga.
Proc Natl Acad Sci U S A, 2021 May 05; 118(19). PMID: 33941690    Free PMC article.