Ultraconserved element

An ultraconserved element (UCE) is a region of the genome that is shared between evolutionarily distant taxa and shows little or no variation between those taxa. These regions and regions adjacent to them (flanking DNA) are useful for tracing the evolutionary history of groups of organisms.{{cite journal |last1=Faircloth |first1=BC |last2=McCormack |first2=JE |last3=Crawford |first3=NG |last4=Harvey |first4=MG |last5=Brumfield |first5=RT |last6=Glenn |first6=TC |title=Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales|journal=Systematic Biology |date=October 2012 |volume=61 |issue=5 |pages=717-26 |doi=10.1093/sysbio/sys004 |pmid=22232343}}{{cite journal |last1=Zhang |first1=Y. Miles |last2=Williams |first2=Jason L. |last3=Lucky |first3=Andrea |title=Understanding UCEs: A Comprehensive Primer on Using Ultraconserved Elements for Arthropod Phylogenomics |journal=Insect Systematics and Diversity |date=3 September 2019 |volume=3 |issue=5 |doi=10.1093/isd/ixz016|doi-access=free }} Another term for ultraconserved element is ultraconserved region (UCR).

The term "ultraconserved element" was originally defined as a genome segment longer than 200 base pairs (bp) that is absolutely conserved, with no insertions or deletions and 100% identity, between orthologous regions of the human, rat, and mouse genomes.{{cite journal | vauthors = Reneker J, Lyons E, Conant GC, Pires JC, Freeling M, Shyu CR, Korkin D | title = Long identical multispecies elements in plant and animal genomes | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 109 | issue = 19 | pages = E1183–E1191 | date = May 2012 | pmid = 22496592 | pmc = 3358895 | doi = 10.1073/pnas.1121356109 | doi-access = free }}{{cite journal |vauthors=Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ, Mattick JS, Haussler D |date=May 2004 |title=Ultraconserved elements in the human genome |journal=Science |volume=304 |issue=5675 |pages=1321–1325 |bibcode=2004Sci...304.1321B |citeseerx=10.1.1.380.9305 |doi=10.1126/science.1098119 |pmid=15131266 |s2cid=2790337}} 481 of these segments have been identified in the human genome. If ribosomal DNA (rDNA regions) are excluded, these range in size from 200 bp to 781 bp. UCEs are found on all human chromosomes except for 21 and Y.

Since its creation, this term's usage has broadened to include more evolutionarily distant species or shorter segments, for example 100 bp instead of 200 bp. By some definitions, segments need not be syntenic between species. Human UCEs also show high conservation with more evolutionarily distant species, such as chicken and fugu. Out of 481 identified human UCEs, approximately 97% align with high identity to the chicken genome, though only 4% of the human genome can be reliably aligned to the chicken genome. Similarly, the same sequences in the fugu genome have 68% identity to human UCEs, despite the human genome only reliably aligning to 1.8% of the fugu genome. Despite often being noncoding DNA,{{cite journal | vauthors = Katzman S, Kern AD, Bejerano G, Fewell G, Fulton L, Wilson RK, Salama SR, Haussler D | display-authors = 6 | title = Human genome ultraconserved elements are ultraselected | journal = Science | volume = 317 | issue = 5840 | pages = 915 | date = August 2007 | pmid = 17702936 | doi = 10.1126/science.1142430 | s2cid = 35322654 | bibcode = 2007Sci...317..915K }} some ultraconserved elements have been found to be transcriptionally active, producing non-coding RNA molecules.{{cite journal | vauthors = Calin GA, Liu CG, Ferracin M, Hyslop T, Spizzo R, Sevignani C, Fabbri M, Cimmino A, Lee EJ, Wojcik SE, Shimizu M, Tili E, Rossi S, Taccioli C, Pichiorri F, Liu X, Zupo S, Herlea V, Gramantieri L, Lanza G, Alder H, Rassenti L, Volinia S, Schmittgen TD, Kipps TJ, Negrini M, Croce CM | display-authors = 6 | title = Ultraconserved regions encoding ncRNAs are altered in human leukemias and carcinomas | journal = Cancer Cell | volume = 12 | issue = 3 | pages = 215–229 | date = September 2007 | pmid = 17785203 | doi = 10.1016/j.ccr.2007.07.027 | doi-access = free }}

Evolution

Researchers originally assumed that perfect conservation of these long stretches of DNA implied evolutionary importance, as these regions appear to have experienced strong negative (purifying) selection for 300-400 million years.{{cite journal | vauthors = Sathirapongsasuti JF, Sathira N, Suzuki Y, Huttenhower C, Sugano S | title = Ultraconserved cDNA segments in the human transcriptome exhibit resistance to folding and implicate function in translation and alternative splicing | journal = Nucleic Acids Research | volume = 39 | issue = 6 | pages = 1967–1979 | date = March 2011 | pmid = 21062826 | pmc = 3064809 | doi = 10.1093/nar/gkq949 }} More recently, this assumption has been replaced by two main hypotheses: that UCEs are created through a reduced negative selection rate, or through reduced mutation rates, also known as a "cold spot" of evolution. Many studies have examined the validity of each hypothesis. The probability of finding ultraconserved elements by chance (under neutral evolution) has been estimated at less than 10−22 in 2.9 billion bases. In support of the cold spot hypothesis, UCEs were found to be mutating 20 fold less than expected under conservative models for neutral mutation rates. This fold change difference in mutation rates was consistent between humans, chimpanzees, and chickens. Ultraconserved elements are not exempt from mutations, as exemplified by the presence of 29,983 polymorphisms in the UCE regions of the human genome assembly GRCh38.{{cite journal | vauthors = Habic A, Mattick JS, Calin GA, Krese R, Konc J, Kunej T | title = Genetic Variations of Ultraconserved Elements in the Human Genome | journal = Omics | volume = 23 | issue = 11 | pages = 549–559 | date = November 2019 | pmid = 31689173 | pmc = 6857462 | doi = 10.1089/omi.2019.0156 }} However, affected phenotypes were only caused by 112 of these polymorphisms, most of which were located in coding regions of the UCEs. A study performed in mice determined that deleting UCEs from the genome did not create obvious deleterious phenotypes, despite deletion of UCEs in proximity to promoters and protein coding genes.{{cite journal | vauthors = Ahituv N, Zhu Y, Visel A, Holt A, Afzal V, Pennacchio LA, Rubin EM | title = Deletion of ultraconserved elements yields viable mice | journal = PLOS Biology | volume = 5 | issue = 9 | pages = e234 | date = September 2007 | pmid = 17803355 | pmc = 1964772 | doi = 10.1371/journal.pbio.0050234 | doi-access = free }} Affected mice were fertile and targeted screens of the nearby coding genes showed no altered phenotype. A separate mouse study demonstrated that ultraconserved enhancers were robust to mutagenesis, concluding that perfect conservation of UCE sequences is not required for their function, which would suggest another reason for the sequence consistency besides evolutionary importance.{{cite journal | vauthors = Snetkova V, Ypsilanti AR, Akiyama JA, Mannion BJ, Plajzer-Frick I, Novak CS, Harrington AN, Pham QT, Kato M, Zhu Y, Godoy J, Meky E, Hunter RD, Shi M, Kvon EZ, Afzal V, Tran S, Rubenstein JL, Visel A, Pennacchio LA, Dickel DE | display-authors = 6 | title = Ultraconserved enhancer function does not require perfect sequence conservation | journal = Nature Genetics | volume = 53 | issue = 4 | pages = 521–528 | date = April 2021 | pmid = 33782603 | pmc = 8038972 | doi = 10.1038/s41588-021-00812-3 }} Computational analysis of human ultraconserved noncoding elements (UCNEs) found that the regions are enriched for A-T sequences and are generally GC poor.{{cite journal | vauthors = Fedorova L, Mulyar OA, Lim J, Fedorov A | title = Nucleotide Composition of Ultra-Conserved Elements Shows Excess of GpC and Depletion of GG and CC Dinucleotides | journal = Genes | volume = 13 | issue = 11 | pages = 2053 | date = November 2022 | pmid = 36360290 | pmc = 9690913 | doi = 10.3390/genes13112053 | doi-access = free }} However, the UNCEs were found to be enriched for CpG, or highly methylated. This may indicate that there is some change to DNA structure in these regions favoring their precise retention, but this possibility has not been validated through testing.

Function

Often, ultraconserved elements are located near transcriptional regulators or developmental genes performing functions such as gene enhancing and splicing regulation.{{cite journal |display-authors=6 |vauthors=Saygin D, Tabib T, Bittar HE, Valenzi E, Sembrat J, Chan SY, Rojas M, Lafyatis R |date=January 2005 |title=Transcriptional profiling of lung cell populations in idiopathic pulmonary arterial hypertension |journal=Pulmonary Circulation |volume=10 |issue=1 |pages=e19 |doi=10.1371/journal.pbio.0030019 |pmc=544543 |pmid=32166015 |doi-access=free }} {{open access}} A study comparing ultraconserved elements between humans and the Japanese puffer fish Takifugu rubripes proposed an importance in vertebrate development.{{cite journal |display-authors=6 |vauthors=Woolfe A, Goodson M, Goode DK, Snell P, McEwen GK, Vavouri T, Smith SF, North P, Callaway H, Kelly K, Walter K, Abnizova I, Gilks W, Edwards YJ, Cooke JE, Elgar G |date=January 2005 |title=Highly conserved non-coding sequences are associated with vertebrate development |journal=PLOS Biology |volume=3 |issue=1 |pages=e7 |doi=10.1371/journal.pbio.0030007 |pmc=526512 |pmid=15630479 |doi-access=free }} {{open access}} Double-knockouts of UCEs near the ARX gene in mice caused a shrunken hippocampus in the brain, though the effect was not lethal.Elizabeth Pennisi (2017) [https://www.science.org/doi/10.1126/science.356.6341.892 Mysterious unchanging DNA finds a purpose in life], Science 02 Jun 2017] Some UCEs are not transcribed, and are referred to as ultraconserved noncoding elements. However, many UCRs in humans are extensively transcribed. A small number of those which are transcribed, known as transcribed UCEs (T-UCEs), have been connected with human carcinomas and leukemias. For example, TUC338 is strongly upregulated in human hepatocellular carcinoma cells.{{cite journal | vauthors = Braconi C, Valeri N, Kogure T, Gasparini P, Huang N, Nuovo GJ, Terracciano L, Croce CM, Patel T | display-authors = 6 | title = Expression and functional role of a transcribed noncoding RNA with an ultraconserved element in hepatocellular carcinoma | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 108 | issue = 2 | pages = 786–791 | date = January 2011 | pmid = 21187392 | pmc = 3021052 | doi = 10.1073/pnas.1011098108 | doi-access = free | bibcode = 2011PNAS..108..786B }} Indeed, UCEs are often affected by copy number variation in cancer cells much more than in healthy contexts, suggesting that altering the copy number of T-UCEs may be deleterious.{{cite journal |vauthors=McCole RB, Fonseka CY, Koren A, Wu CT |date=October 2014 |title=Abnormal dosage of ultraconserved elements is highly disfavored in healthy cells but not cancer cells |journal=PLOS Genetics |volume=10 |issue=10 |pages=e1004646 |doi=10.1371/journal.pgen.1004646 |pmc=4207606 |pmid=25340765 |doi-access=free }}{{cite journal |vauthors=Derti A, Roth FP, Church GM, Wu CT |date=October 2006 |title=Mammalian ultraconserved elements are strongly depleted among segmental duplications and copy number variants |journal=Nature Genetics |volume=38 |issue=10 |pages=1216–1220 |doi=10.1038/ng1888 |pmid=16998490 |s2cid=10671674}}{{cite journal |vauthors=Chiang CW, Derti A, Schwartz D, Chou MF, Hirschhorn JN, Wu CT |date=December 2008 |title=Ultraconserved elements: analyses of dosage sensitivity, motifs and boundaries |journal=Genetics |volume=180 |issue=4 |pages=2277–2293 |doi=10.1534/genetics.108.096537 |pmc=2600958 |pmid=18957701}}

Role in human disease

Research has demonstrated that T-UCRs have a tissue-specific expression, and a differential expression profile between tumors and other diseases.{{cite journal | vauthors = Pereira Zambalde E, Mathias C, Rodrigues AC, de Souza Fonseca Ribeiro EM, Fiori Gradia D, Calin GA, Carvalho de Oliveira J | title = Highlighting transcribed ultraconserved regions in human diseases | journal = Wiley Interdisciplinary Reviews. RNA | volume = 11 | issue = 2 | pages = e1567 | date = March 2020 | pmid = 31489780 | doi = 10.1002/wrna.1567 | s2cid = 201844414 }} The tables below highlight transcripts and polymorphisms within UCRs that have been shown to contribute to human diseases. For example, UCRs tend to accumulate less mutations than flanking segments, in both neoplastic and non-neoplastic samples from persons with hereditary non-polyposis colorectal cancer.{{cite journal |display-authors=6 |vauthors=De Grassi A, Segala C, Iannelli F, Volorio S, Bertario L, Radice P, Bernard L, Ciccarelli FD |date=January 2010 |title=Ultradeep sequencing of a human ultraconserved region reveals somatic and constitutional genomic instability |journal=PLOS Biology |volume=8 |issue=1 |pages=e1000275 |doi=10.1371/journal.pbio.1000275 |pmc=2794366 |pmid=20052272 |veditors=Hastie N |doi-access=free }}

= Phenotype-associated polymorphisms within ultraconserved elements =

class="wikitable"

|Polymorphism name

|Associated phenotype description

|Source

rs17105335

|Amyotrophic lateral sclerosis

|Cronin et al. (2008){{cite journal | vauthors = Cronin S, Berger S, Ding J, Schymick JC, Washecka N, Hernandez DG, Greenway MJ, Bradley DG, Traynor BJ, Hardiman O | display-authors = 6 | title = A genome-wide association study of sporadic ALS in a homogenous Irish population | journal = Human Molecular Genetics | volume = 17 | issue = 5 | pages = 768–774 | date = March 2008 | pmid = 18057069 | doi = 10.1093/hmg/ddm361 | doi-access = free }}

rs2020906

|Lynch syndrome

|Hansen et al. (2014){{cite journal | vauthors = Hansen MF, Neckmann U, Lavik LA, Vold T, Gilde B, Toft RK, Sjursen W | title = A massive parallel sequencing workflow for diagnostic genetic testing of mismatch repair genes | journal = Molecular Genetics & Genomic Medicine | volume = 2 | issue = 2 | pages = 186–200 | date = March 2014 | pmid = 24689082 | pmc = 3960061 | doi = 10.1002/mgg3.62 }}

rs10496382

|Height

|Chiang et al. (2012){{cite journal | vauthors = Chiang CW, Liu CT, Lettre G, Lange LA, Jorgensen NW, Keating BJ, Vedantam S, Nock NL, Franceschini N, Reiner AP, Demerath EW, Boerwinkle E, Rotter JI, Wilson JG, North KE, Papanicolaou GJ, Cupples LA, Murabito JM, Hirschhorn JN | display-authors = 6 | title = Ultraconserved elements in the human genome: association and transmission analyses of highly constrained single-nucleotide polymorphisms | journal = Genetics | volume = 192 | issue = 1 | pages = 253–266 | date = September 2012 | pmid = 22714408 | pmc = 3430540 | doi = 10.1534/genetics.112.141945 }}

rs13382811

|Severe myopia

|Khor et al. (2013){{cite journal | vauthors = Khor CC, Miyake M, Chen LJ, Shi Y, Barathi VA, Qiao F, Nakata I, Yamashiro K, Zhou X, Tam PO, Cheng CY, Tai ES, Vithana EN, Aung T, Teo YY, Wong TY, Moriyama M, Ohno-Matsui K, Mochizuki M, Matsuda F, Yong RY, Yap EP, Yang Z, Pang CP, Saw SM, Yoshimura N | display-authors = 6 | title = Genome-wide association study identifies ZFHX1B as a susceptibility locus for severe myopia | journal = Human Molecular Genetics | volume = 22 | issue = 25 | pages = 5288–5294 | date = December 2013 | pmid = 23933737 | doi = 10.1093/hmg/ddt385 | doi-access = free }}

rs104893634

|Vertical talus congenital

|Dobbs et al. (2006);{{cite journal | vauthors = Dobbs MB, Gurnett CA, Pierce B, Exner GU, Robarge J, Morcuende JA, Cole WG, Templeton PA, Foster B, Bowcock AM | display-authors = 6 | title = HOXD10 M319K mutation in a family with isolated congenital vertical talus | journal = Journal of Orthopaedic Research | volume = 24 | issue = 3 | pages = 448–453 | date = March 2006 | pmid = 16450407 | doi = 10.1002/jor.20052 | s2cid = 28670628 | doi-access = free }} Shrimpton et al. (2004)

rs2307121

|Central corneal thickness

|Lu et al. (2013){{cite journal | vauthors = Lu Y, Vitart V, Burdon KP, Khor CC, Bykhovskaya Y, Mirshahi A, Hewitt AW, Koehn D, Hysi PG, Ramdas WD, Zeller T, Vithana EN, Cornes BK, Tay WT, Tai ES, Cheng CY, Liu J, Foo JN, Saw SM, Thorleifsson G, Stefansson K, Dimasi DP, Mills RA, Mountain J, Ang W, Hoehn R, Verhoeven VJ, Grus F, Wolfs R, Castagne R, Lackner KJ, Springelkamp H, Yang J, Jonasson F, Leung DY, Chen LJ, Tham CC, Rudan I, Vatavuk Z, Hayward C, Gibson J, Cree AJ, MacLeod A, Ennis S, Polasek O, Campbell H, Wilson JF, Viswanathan AC, Fleck B, Li X, Siscovick D, Taylor KD, Rotter JI, Yazar S, Ulmer M, Li J, Yaspan BL, Ozel AB, Richards JE, Moroi SE, Haines JL, Kang JH, Pasquale LR, Allingham RR, Ashley-Koch A, Mitchell P, Wang JJ, Wright AF, Pennell C, Spector TD, Young TL, Klaver CC, Martin NG, Montgomery GW, Anderson MG, Aung T, Willoughby CE, Wiggs JL, Pang CP, Thorsteinsdottir U, Lotery AJ, Hammond CJ, van Duijn CM, Hauser MA, Rabinowitz YS, Pfeiffer N, Mackey DA, Craig JE, Macgregor S, Wong TY | display-authors = 6 | title = Genome-wide association analyses identify multiple loci associated with central corneal thickness and keratoconus | journal = Nature Genetics | volume = 45 | issue = 2 | pages = 155–163 | date = February 2013 | pmid = 23291589 | pmc = 3720123 | doi = 10.1038/ng.2506 }}

rs587777277

|Bosch-Boonstra-Schaaf optic atrophy syndrome

|Bosch et al. (2014){{cite journal | vauthors = Bosch DG, Boonstra FN, Gonzaga-Jauregui C, Xu M, de Ligt J, Jhangiani S, Wiszniewski W, Muzny DM, Yntema HG, Pfundt R, Vissers LE, Spruijt L, Blokland EA, Chen CA, Lewis RA, Tsai SY, Gibbs RA, Tsai MJ, Lupski JR, Zoghbi HY, Cremers FP, de Vries BB, Schaaf CP | display-authors = 6 | title = NR2F1 mutations cause optic atrophy with intellectual disability | journal = American Journal of Human Genetics | volume = 94 | issue = 2 | pages = 303–309 | date = February 2014 | pmid = 24462372 | pmc = 3928641 | doi = 10.1016/j.ajhg.2014.01.002 }}

rs587777275

|Bosch-Boonstra-Schaaf optic atrophy syndrome

|Bosch et al. (2014)

rs587777274

|Bosch-Boonstra-Schaaf optic atrophy syndrome

|Bosch et al. (2014)

rs387906239

|Familial adenomatous polyposis 1 attenuated

|Soravia et al. (1999){{cite journal | vauthors = Soravia C, Sugg SL, Berk T, Mitri A, Cheng H, Gallinger S, Cohen Z, Asa SL, Bapat BV | display-authors = 6 | title = Familial adenomatous polyposis-associated thyroid cancer: a clinical, pathological, and molecular genetics study | journal = The American Journal of Pathology | volume = 154 | issue = 1 | pages = 127–135 | date = January 1999 | pmid = 9916927 | pmc = 1853451 | doi = 10.1016/S0002-9440(10)65259-5 }}

rs3797704

|No association with breast cancer

|Chang et al. (2016){{cite journal | vauthors = Chang YS, Lin CY, Yang SF, Ho CM, Chang JG | title = Analysing the mutational status of adenomatous polyposis coli (APC) gene in breast cancer | journal = Cancer Cell International | volume = 16 | pages = 23 | date = 2016-03-28 | pmid = 27028212 | pmc = 4810512 | doi = 10.1186/s12935-016-0297-2 | doi-access = free }}

rs387906232

|Familial adenomatous polyposis 1

|Fodde et al. (1992){{cite journal | vauthors = Fodde R, van der Luijt R, Wijnen J, Tops C, van der Klift H, van Leeuwen-Cornelisse I, Griffioen G, Vasen H, Khan PM | display-authors = 6 | title = Eight novel inactivating germ line mutations at the APC gene identified by denaturing gradient gel electrophoresis | journal = Genomics | volume = 13 | issue = 4 | pages = 1162–1168 | date = August 1992 | pmid = 1324223 | doi = 10.1016/0888-7543(92)90032-n }}

rs387906237

|Familial adenomatous polyposis 1 attenuated

|Curia et al. (1998){{cite journal | vauthors = Curia MC, Esposito DL, Aceto G, Palmirotta R, Crognale S, Valanzano R, Ficari F, Tonelli F, Battista P, Mariani-Costantini R, Cama A | display-authors = 6 | title = Transcript dosage effect in familial adenomatous polyposis: model offered by two kindreds with exon 9 APC gene mutations | journal = Human Mutation | volume = 11 | issue = 3 | pages = 197–201 | date = 1998 | pmid = 9521420 | doi = 10.1002/(SICI)1098-1004(1998)11:3<197::AID-HUMU3>3.0.CO;2-F | s2cid = 7241178 }}

rs121434591

|Distal myopathy

|Senderek et al. (2009)

rs587777300

|Amyotrophic lateral sclerosis 21

|Johnson et al. (2014){{cite journal | vauthors = Johnson JO, Pioro EP, Boehringer A, Chia R, Feit H, Renton AE, Pliner HA, Abramzon Y, Marangi G, Winborn BJ, Gibbs JR, Nalls MA, Morgan S, Shoai M, Hardy J, Pittman A, Orrell RW, Malaspina A, Sidle KC, Fratta P, Harms MB, Baloh RH, Pestronk A, Weihl CC, Rogaeva E, Zinman L, Drory VE, Borghero G, Mora G, Calvo A, Rothstein JD, Drepper C, Sendtner M, Singleton AB, Taylor JP, Cookson MR, Restagno G, Sabatelli M, Bowser R, Chiò A, Traynor BJ | display-authors = 6 | title = Mutations in the Matrin 3 gene cause familial amyotrophic lateral sclerosis | journal = Nature Neuroscience | volume = 17 | issue = 5 | pages = 664–666 | date = May 2014 | pmid = 24686783 | pmc = 4000579 | doi = 10.1038/nn.3688 }}

rs863223403

|Au-Kline syndrome

|Au et al. (2015){{cite journal | vauthors = Au PY, You J, Caluseriu O, Schwartzentruber J, Majewski J, Bernier FP, Ferguson M, Valle D, Parboosingh JS, Sobreira N, Innes AM, Kline AD | display-authors = 6 | title = GeneMatcher aids in the identification of a new malformation syndrome with intellectual disability, unique facial dysmorphisms, and skeletal and connective tissue abnormalities caused by de novo variants in HNRNPK | journal = Human Mutation | volume = 36 | issue = 10 | pages = 1009–1014 | date = October 2015 | pmid = 26173930 | pmc = 4589226 | doi = 10.1002/humu.22837 }}

rs121917900

|Cockayne syndrome B

|Mallery et al. (1998){{cite journal | vauthors = Mallery DL, Tanganelli B, Colella S, Steingrimsdottir H, van Gool AJ, Troelstra C, Stefanini M, Lehmann AR | display-authors = 6 | title = Molecular analysis of mutations in the CSB (ERCC6) gene in patients with Cockayne syndrome | journal = American Journal of Human Genetics | volume = 62 | issue = 1 | pages = 77–85 | date = January 1998 | pmid = 9443879 | pmc = 1376810 | doi = 10.1086/301686 }}

rs75462234

|Papillorenal syndrome

|Schimmenti et al. (1999){{cite journal | vauthors = Schimmenti LA, Shim HH, Wirtschafter JD, Panzarino VA, Kashtan CE, Kirkpatrick SJ, Wargowski DS, France TD, Michel E, Dobyns WB | display-authors = 6 | title = Homonucleotide expansion and contraction mutations of PAX2 and inclusion of Chiari 1 malformation as part of renal-coloboma syndrome | journal = Human Mutation | volume = 14 | issue = 5 | pages = 369–376 | date = 1999 | pmid = 10533062 | doi = 10.1002/(SICI)1098-1004(199911)14:5<369::AID-HUMU2>3.0.CO;2-E | s2cid = 25564812 | doi-access = free }}

rs77453353

|Renal coloboma syndrome

|Amiel et al. (2000){{cite journal | vauthors = Amiel J, Audollent S, Joly D, Dureau P, Salomon R, Tellier AL, Augé J, Bouissou F, Antignac C, Gubler MC, Eccles MR, Munnich A, Vekemans M, Lyonnet S, Attié-Bitach T | display-authors = 6 | title = PAX2 mutations in renal-coloboma syndrome: mutational hotspot and germline mosaicism | journal = European Journal of Human Genetics | volume = 8 | issue = 11 | pages = 820–826 | date = November 2000 | pmid = 11093271 | doi = 10.1038/sj.ejhg.5200539 | s2cid = 30359554 | doi-access = free }}

rs76675173

|Papillorenal syndrome

|Schimmenti et al. (1997){{cite journal | vauthors = Schimmenti LA, Cunliffe HE, McNoe LA, Ward TA, French MC, Shim HH, Zhang YH, Proesmans W, Leys A, Byerly KA, Braddock SR, Masuno M, Imaizumi K, Devriendt K, Eccles MR | display-authors = 6 | title = Further delineation of renal-coloboma syndrome in patients with extreme variability of phenotype and identical PAX2 mutations | journal = American Journal of Human Genetics | volume = 60 | issue = 4 | pages = 869–878 | date = April 1997 | pmid = 9106533 | pmc = 1712484 }}

rs587777708

|Focal segmental glomerulosclerosis 7

|Barua et al. (2014){{cite journal | vauthors = Barua M, Stellacci E, Stella L, Weins A, Genovese G, Muto V, Caputo V, Toka HR, Charoonratana VT, Tartaglia M, Pollak MR | display-authors = 6 | title = Mutations in PAX2 associate with adult-onset FSGS | journal = Journal of the American Society of Nephrology | volume = 25 | issue = 9 | pages = 1942–1953 | date = September 2014 | pmid = 24676634 | pmc = 4147972 | doi = 10.1681/ASN.2013070686 }}

rs11190870

|Adolescent idiopathic scoliosis, no association with breast cancer

|Chettier et al. (2015);{{cite journal | vauthors = Chettier R, Nelson L, Ogilvie JW, Albertsen HM, Ward K | title = Haplotypes at LBX1 have distinct inheritance patterns with opposite effects in adolescent idiopathic scoliosis | journal = PLOS ONE | volume = 10 | issue = 2 | pages = e0117708 | date = 2015-02-12 | pmid = 25675428 | pmc = 4326419 | doi = 10.1371/journal.pone.0117708 | bibcode = 2015PLoSO..1017708C | veditors = Fang S | doi-access = free }} Gao et al. (2013);{{cite journal | vauthors = Gao W, Peng Y, Liang G, Liang A, Ye W, Zhang L, Sharma S, Su P, Huang D | display-authors = 6 | title = Association between common variants near LBX1 and adolescent idiopathic scoliosis replicated in the Chinese Han population | journal = PLOS ONE | volume = 8 | issue = 1 | pages = e53234 | date = 2013-01-04 | pmid = 23308168 | pmc = 3537668 | doi = 10.1371/journal.pone.0053234 | bibcode = 2013PLoSO...853234G | doi-access = free }} Grauers et al. (2015);{{cite journal | vauthors = Grauers A, Wang J, Einarsdottir E, Simony A, Danielsson A, Åkesson K, Ohlin A, Halldin K, Grabowski P, Tenne M, Laivuori H, Dahlman I, Andersen M, Christensen SB, Karlsson MK, Jiao H, Kere J, Gerdhem P | display-authors = 6 | title = Candidate gene analysis and exome sequencing confirm LBX1 as a susceptibility gene for idiopathic scoliosis | journal = The Spine Journal | volume = 15 | issue = 10 | pages = 2239–2246 | date = October 2015 | pmid = 25987191 | doi = 10.1016/j.spinee.2015.05.013 | hdl = 10616/44765 | hdl-access = free }} Jiang et al. (2013);{{cite journal | vauthors = Jiang H, Qiu X, Dai J, Yan H, Zhu Z, Qian B, Qiu Y | title = Association of rs11190870 near LBX1 with adolescent idiopathic scoliosis susceptibility in a Han Chinese population | journal = European Spine Journal | volume = 22 | issue = 2 | pages = 282–286 | date = February 2013 | pmid = 23096252 | pmc = 3555620 | doi = 10.1007/s00586-012-2532-4 }} Londono et al. (2014);{{cite journal | vauthors = Londono D, Kou I, Johnson TA, Sharma S, Ogura Y, Tsunoda T, Takahashi A, Matsumoto M, Herring JA, Lam TP, Wang X, Tam EM, Song YQ, Fan YH, Chan D, Cheah KS, Qiu X, Jiang H, Huang D, Su P, Sham P, Cheung KM, Luk KD, Gordon D, Qiu Y, Cheng J, Tang N, Ikegawa S, Wise CA | display-authors = 6 | title = A meta-analysis identifies adolescent idiopathic scoliosis association with LBX1 locus in multiple ethnic groups | journal = Journal of Medical Genetics | volume = 51 | issue = 6 | pages = 401–406 | date = June 2014 | pmid = 24721834 | doi = 10.1136/jmedgenet-2013-102067 | s2cid = 23646905 }} Miyake et al. (2013);{{cite journal | vauthors = Miyake A, Kou I, Takahashi Y, Johnson TA, Ogura Y, Dai J, Qiu X, Takahashi A, Jiang H, Yan H, Kono K, Kawakami N, Uno K, Ito M, Minami S, Yanagida H, Taneichi H, Hosono N, Tsuji T, Suzuki T, Sudo H, Kotani T, Yonezawa I, Kubo M, Tsunoda T, Watanabe K, Chiba K, Toyama Y, Qiu Y, Matsumoto M, Ikegawa S | display-authors = 6 | title = Identification of a susceptibility locus for severe adolescent idiopathic scoliosis on chromosome 17q24.3 | journal = PLOS ONE | volume = 8 | issue = 9 | pages = e72802 | date = 2013-09-04 | pmid = 24023777 | pmc = 3762929 | doi = 10.1371/journal.pone.0072802 | bibcode = 2013PLoSO...872802M | doi-access = free }} Shen et al. (2011);{{cite journal | vauthors = Jiang Y, Ben Q, Shen H, Lu W, Zhang Y, Zhu J | title = Diabetes mellitus and incidence and mortality of colorectal cancer: a systematic review and meta-analysis of cohort studies | journal = European Journal of Epidemiology | volume = 26 | issue = 11 | pages = 863–876 | date = November 2011 | pmid = 21938478 | doi = 10.1007/s10654-011-9617-y | s2cid = 99605 }} Takahashi et al. (2011){{cite journal | vauthors = Takahashi Y, Kou I, Takahashi A, Johnson TA, Kono K, Kawakami N, Uno K, Ito M, Minami S, Yanagida H, Taneichi H, Tsuji T, Suzuki T, Sudo H, Kotani T, Watanabe K, Chiba K, Hosono N, Kamatani N, Tsunoda T, Toyama Y, Kubo M, Matsumoto M, Ikegawa S | display-authors = 6 | title = A genome-wide association study identifies common variants near LBX1 associated with adolescent idiopathic scoliosis | journal = Nature Genetics | volume = 43 | issue = 12 | pages = 1237–1240 | date = October 2011 | pmid = 22019779 | doi = 10.1038/ng.974 | s2cid = 7533298 }}

rs724159963

|Peroxisomal fatty acyl-CoA reductase 1 disorder

|Buchert et al. (2014){{cite journal | vauthors = Buchert R, Tawamie H, Smith C, Uebe S, Innes AM, Al Hallak B, Ekici AB, Sticht H, Schwarze B, Lamont RE, Parboosingh JS, Bernier FP, Abou Jamra R | display-authors = 6 | title = A peroxisomal disorder of severe intellectual disability, epilepsy, and cataracts due to fatty acyl-CoA reductase 1 deficiency | language = English | journal = American Journal of Human Genetics | volume = 95 | issue = 5 | pages = 602–610 | date = November 2014 | pmid = 25439727 | pmc = 4225589 | doi = 10.1016/j.ajhg.2014.10.003 }}

rs16932455

|Capecitabine sensitivity

|O'Donnell et al. (2012){{cite journal | vauthors = O'Donnell PH, Stark AL, Gamazon ER, Wheeler HE, McIlwee BE, Gorsic L, Im HK, Huang RS, Cox NJ, Dolan ME | display-authors = 6 | title = Identification of novel germline polymorphisms governing capecitabine sensitivity | journal = Cancer | volume = 118 | issue = 16 | pages = 4063–4073 | date = August 2012 | pmid = 22864933 | pmc = 3413892 | doi = 10.1002/cncr.26737 }}

rs997295

|Motion sickness; BMI

|De et al. (2015);{{cite journal | vauthors = De R, Verma SS, Drenos F, Holzinger ER, Holmes MV, Hall MA, Crosslin DR, Carrell DS, Hakonarson H, Jarvik G, Larson E, Pacheco JA, Rasmussen-Torvik LJ, Moore CB, Asselbergs FW, Moore JH, Ritchie MD, Keating BJ, Gilbert-Diamond D | display-authors = 6 | title = Identifying gene-gene interactions that are highly associated with Body Mass Index using Quantitative Multifactor Dimensionality Reduction (QMDR) | journal = BioData Mining | volume = 8 | issue = 1 | pages = 41 | date = June 2015 | pmid = 26674805 | pmc = 4678717 | doi = 10.1186/s13040-015-0074-0 | doi-access = free }} Guo et al. (2013);{{cite journal | vauthors = Guo Y, Lanktree MB, Taylor KC, Hakonarson H, Lange LA, Keating BJ | title = Gene-centric meta-analyses of 108 912 individuals confirm known body mass index loci and reveal three novel signals | journal = Human Molecular Genetics | volume = 22 | issue = 1 | pages = 184–201 | date = January 2013 | pmid = 23001569 | pmc = 3522401 | doi = 10.1093/hmg/dds396 }} Hromatka et al.{{cite journal | vauthors = Hromatka BS, Tung JY, Kiefer AK, Do CB, Hinds DA, Eriksson N | title = Genetic variants associated with motion sickness point to roles for inner ear development, neurological processes and glucose homeostasis | journal = Human Molecular Genetics | volume = 24 | issue = 9 | pages = 2700–2708 | date = May 2015 | pmid = 25628336 | pmc = 4383869 | doi = 10.1093/hmg/ddv028 }}

rs587777373

|Congenital heart defects multiple types 4

|Al Turki et al. (2014){{cite journal | vauthors = Al Turki S, Manickaraj AK, Mercer CL, Gerety SS, Hitz MP, Lindsay S, D'Alessandro LC, Swaminathan GJ, Bentham J, Arndt AK, Louw J, Low J, Breckpot J, Gewillig M, Thienpont B, Abdul-Khaliq H, Harnack C, Hoff K, Kramer HH, Schubert S, Siebert R, Toka O, Cosgrove C, Watkins H, Lucassen AM, O'Kelly IM, Salmon AP, Bu'lock FA, Granados-Riveron J, Setchfield K, Thornborough C, Brook JD, Mulder B, Klaassen S, Bhattacharya S, Devriendt K, Fitzpatrick DF, Wilson DI, Mital S, Hurles ME | display-authors = 6 | title = Rare variants in NR2F2 cause congenital heart defects in humans | journal = American Journal of Human Genetics | volume = 94 | issue = 4 | pages = 574–585 | date = April 2014 | pmid = 24702954 | pmc = 3980509 | doi = 10.1016/j.ajhg.2014.03.007 }}

rs398123839

|Duchenne muscular dystrophy

|Hofstra et al. (2004);{{cite journal | vauthors = Hofstra RM, Mulder IM, Vossen R, de Koning-Gans PA, Kraak M, Ginjaar IB, van der Hout AH, Bakker E, Buys CH, van Ommen GJ, van Essen AJ, den Dunnen JT | display-authors = 6 | title = DGGE-based whole-gene mutation scanning of the dystrophin gene in Duchenne and Becker muscular dystrophy patients | journal = Human Mutation | volume = 23 | issue = 1 | pages = 57–66 | date = January 2004 | pmid = 14695533 | doi = 10.1002/humu.10283 | s2cid = 36020079 | doi-access = free }} Roberts et al. (1992){{cite journal | vauthors = Roberts RG, Bobrow M, Bentley DR | title = Point mutations in the dystrophin gene | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 89 | issue = 6 | pages = 2331–2335 | date = March 1992 | pmid = 1549596 | pmc = 48651 | doi = 10.1073/pnas.89.6.2331 | bibcode = 1992PNAS...89.2331R | doi-access = free }}

rs863224976

|Becker muscular dystrophy

|Tuffery-Giraud et al. (2005){{cite journal | vauthors = Tuffery-Giraud S, Saquet C, Thorel D, Disset A, Rivier F, Malcolm S, Claustres M | title = Mutation spectrum leading to an attenuated phenotype in dystrophinopathies | journal = European Journal of Human Genetics | volume = 13 | issue = 12 | pages = 1254–1260 | date = December 2005 | pmid = 16077730 | doi = 10.1038/sj.ejhg.5201478 | s2cid = 22585201 | doi-access = free }}

rs132630295

|Spastic paraplegia 2 X-linked

|Gorman et al. (2007){{cite journal | vauthors = Gorman MP, Golomb MR, Walsh LE, Hobson GM, Garbern JY, Kinkel RP, Darras BT, Urion DK, Eksioglu YZ | display-authors = 6 | title = Steroid-responsive neurologic relapses in a child with a proteolipid protein-1 mutation | journal = Neurology | volume = 68 | issue = 16 | pages = 1305–1307 | date = April 2007 | pmid = 17438221 | doi = 10.1212/01.wnl.0000259522.49388.53 | s2cid = 45639125 }}

rs132630287

|Spastic paraplegia 2 X-linked

|Saugier-Veber et al. (1994){{cite journal | vauthors = Saugier-Veber P, Munnich A, Bonneau D, Rozet JM, Le Merrer M, Gil R, Boespflug-Tanguy O | title = X-linked spastic paraplegia and Pelizaeus-Merzbacher disease are allelic disorders at the proteolipid protein locus | journal = Nature Genetics | volume = 6 | issue = 3 | pages = 257–262 | date = March 1994 | pmid = 8012387 | doi = 10.1038/ng0394-257 | s2cid = 13607673 }}

rs132630292

|Pelizaeus/Merzbacher disease atypical

|Hodes et al. (1997){{cite journal | vauthors = Hodes ME, Blank CA, Pratt VM, Morales J, Napier J, Dlouhy SR | title = Nonsense mutation in exon 3 of the proteolipid protein gene (PLP) in a family with an unusual form of Pelizaeus-Merzbacher disease | journal = American Journal of Medical Genetics | volume = 69 | issue = 2 | pages = 121–125 | date = March 1997 | doi = 10.1002/(SICI)1096-8628(19970317)69:2<121::AID-AJMG2>3.0.CO;2-S | pmid = 9056547 | url = https://pubmed.ncbi.nlm.nih.gov/9056547 }}

rs137852350

|Mental retardation X-linked 94

|Wu et al. (2007){{cite journal | vauthors = Wu Y, Arai AC, Rumbaugh G, Srivastava AK, Turner G, Hayashi T, Suzuki E, Jiang Y, Zhang L, Rodriguez J, Boyle J, Tarpey P, Raymond FL, Nevelsteen J, Froyen G, Stratton M, Futreal A, Gecz J, Stevenson R, Schwartz CE, Valle D, Huganir RL, Wang T | display-authors = 6 | title = Mutations in ionotropic AMPA receptor 3 alter channel properties and are associated with moderate cognitive impairment in humans | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 104 | issue = 46 | pages = 18163–18168 | date = November 2007 | pmid = 17989220 | pmc = 2084314 | doi = 10.1073/pnas.0708699104 | bibcode = 2007PNAS..10418163W | doi-access = free }}

rs122459149

|Emery-Dreifuss muscular dystrophy 6 X-linked

|Gueneau et al. (2009);{{cite journal | vauthors = Gueneau L, Bertrand AT, Jais JP, Salih MA, Stojkovic T, Wehnert M, Hoeltzenbein M, Spuler S, Saitoh S, Verschueren A, Tranchant C, Beuvin M, Lacene E, Romero NB, Heath S, Zelenika D, Voit T, Eymard B, Ben Yaou R, Bonne G | display-authors = 6 | title = Mutations of the FHL1 gene cause Emery-Dreifuss muscular dystrophy | journal = American Journal of Human Genetics | volume = 85 | issue = 3 | pages = 338–353 | date = September 2009 | pmid = 19716112 | pmc = 2771595 | doi = 10.1016/j.ajhg.2009.07.015 }} Knoblauch et al. (2010){{cite journal | vauthors = Knoblauch H, Geier C, Adams S, Budde B, Rudolph A, Zacharias U, Schulz-Menger J, Spuler A, Yaou RB, Nürnberg P, Voit T, Bonne G, Spuler S | display-authors = 6 | title = Contractures and hypertrophic cardiomyopathy in a novel FHL1 mutation | journal = Annals of Neurology | volume = 67 | issue = 1 | pages = 136–140 | date = January 2010 | pmid = 20186852 | doi = 10.1002/ana.21839 | s2cid = 30441775 }}

rs122458141

|Myopathy X-linked with postural muscle atrophy

|Schoser et al. (2009);{{cite journal | vauthors = Schoser B, Goebel HH, Janisch I, Quasthoff S, Rother J, Bergmann M, Müller-Felber W, Windpassinger C | display-authors = 6 | title = Consequences of mutations within the C terminus of the FHL1 gene | journal = Neurology | volume = 73 | issue = 7 | pages = 543–551 | date = August 2009 | pmid = 19687455 | doi = 10.1212/WNL.0b013e3181b2a4b3 | s2cid = 13107330 }} Windpassinger et al. (2008){{cite journal | vauthors = Windpassinger C, Schoser B, Straub V, Hochmeister S, Noor A, Lohberger B, Farra N, Petek E, Schwarzbraun T, Ofner L, Löscher WN, Wagner K, Lochmüller H, Vincent JB, Quasthoff S | display-authors = 6 | title = An X-linked myopathy with postural muscle atrophy and generalized hypertrophy, termed XMPMA, is caused by mutations in FHL1 | language = English | journal = American Journal of Human Genetics | volume = 82 | issue = 1 | pages = 88–99 | date = January 2008 | pmid = 18179888 | pmc = 2253986 | doi = 10.1016/j.ajhg.2007.09.004 }}

rs786200914

|Myopathy X-linked with postural muscle atrophy

|Schoser et al. (2009)

rs267606811

|Myopathy X-linked with postural muscle atrophy

|Windpassinger et al. (2008)

rs62621672

|Rett syndrome (nonpathogenic variant)

|Zahorakova et al. (2007){{cite journal | vauthors = Zahorakova D, Rosipal R, Hadac J, Zumrova A, Bzduch V, Misovicova N, Baxova A, Zeman J, Martasek P | display-authors = 6 | title = Mutation analysis of the MECP2 gene in patients of Slavic origin with Rett syndrome: novel mutations and polymorphisms | journal = Journal of Human Genetics | volume = 52 | issue = 4 | pages = 342–348 | date = 2007 | pmid = 17387578 | doi = 10.1007/s10038-007-0121-x | s2cid = 7962500 | doi-access = free }}

See also

References

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