Imperial College London

Dr Natalie C Butterfield

Faculty of MedicineDepartment of Metabolism, Digestion and Reproduction

Research Associate
 
 
 
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Contact

 

+44 (0)20 3313 8432natalie.butterfield Website

 
 
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Location

 

10N2Commonwealth BuildingHammersmith Campus

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Summary

 

Publications

Publication Type
Year
to

26 results found

Kooblall KG, Stevenson M, Stewart M, Harris L, Zalucki O, Dewhurst H, Butterfield N, Leng H, Hough TA, Ma D, Siow B, Potter P, Cox RD, Brown SDM, Horwood N, Wright B, Lockstone H, Buck D, Vincent TL, Hannan FM, Bassett JHD, Williams GR, Lines KE, Piper M, Wells S, Teboul L, Hennekam RC, Thakker RVet al., 2023, A Mouse Model with a Frameshift Mutation in the Nuclear Factor I/X (<i>NFIX</i>) Gene Has Phenotypic Features of Marshall-Smith Syndrome, JBMR PLUS, Vol: 7

Journal article

Youlten SE, Kemp JP, Logan JG, Ghirardello EJ, Sergio CM, Dack MRG, Guilfoyle SE, Leitch VD, Butterfield NC, Komla-Ebri D, Chai RC, Corr AP, Smith JT, Mohanty ST, Morris JA, McDonald MM, Quinn JMW, McGlade AR, Bartonicek N, Jansson M, Hatzikotoulas K, Irving MD, Beleza-Meireles A, Rivadeneira F, Duncan E, Richards JB, Adams DJ, Lelliott CJ, Brink R, Phan TG, Eisman JA, Evans DM, Zeggini E, Baldock PA, Bassett JHD, Williams GR, Croucher PIet al., 2021, Osteocyte transcriptome mapping identifies a molecular landscape controlling skeletal homeostasis and susceptibility to skeletal disease, Nature Communications, Vol: 12, Pages: 1-21, ISSN: 2041-1723

Osteocytes are master regulators of the skeleton. We mapped the transcriptome of osteocytes from different skeletal sites, across age and sexes in mice to reveal genes and molecular programs that control this complex cellular-network. We define an osteocyte transcriptome signature of 1239 genes that distinguishes osteocytes from other cells. 77% have no previously known role in the skeleton and are enriched for genes regulating neuronal network formation, suggesting this programme is important in osteocyte communication. We evaluated 19 skeletal parameters in 733 knockout mouse lines and reveal 26 osteocyte transcriptome signature genes that control bone structure and function. We showed osteocyte transcriptome signature genes are enriched for human orthologs that cause monogenic skeletal disorders (P = 2.4 × 10−22) and are associated with the polygenic diseases osteoporosis (P = 1.8 × 10−13) and osteoarthritis (P = 1.6 × 10−7). Thus, we reveal the molecular landscape that regulates osteocyte network formation and function and establish the importance of osteocytes in human skeletal disease.

Journal article

McDonald MM, Khoo WH, Ng PY, Xiao Y, Zamerli J, Thatcher P, Kyaw W, Pathmanandavel K, Grootveld AK, Moran I, Butt D, Nguyen A, Corr A, Warren S, Biro M, Butterfield NC, Guilfoyle SE, Komla-Ebri D, Dack MRG, Dewhurst HF, Logan JG, Li Y, Mohanty ST, Byrne N, Terry RL, Simic MK, Chai R, Quinn JMW, Youlten SE, Pettitt JA, Abi-Hanna D, Jain R, Weninger W, Lundberg M, Sun S, Ebetino FH, Timpson P, Lee WM, Baldock PA, Rogers MJ, Brink R, Williams GR, Bassett JHD, Kemp JP, Pavlos NJ, Croucher P, Phan TGet al., 2021, Osteoclasts recycle via osteomorphs during RANKL-stimulated bone resorption, Cell, Vol: 184, Pages: 1330-1347.e13, ISSN: 0092-8674

Osteoclasts are large multinucleated bone-resorbing cells formed by the fusion of monocyte/macrophage-derived precursors that are thought to undergo apoptosis once resorption is complete. Here, by intravital imaging, we reveal that RANKL-stimulated osteoclasts have an alternative cell fate in which they fission into daughter cells called osteomorphs. Inhibiting RANKL blocked this cellular recycling and resulted in osteomorph accumulation. Single-cell RNA sequencing showed that osteomorphs are transcriptionally distinct from osteoclasts and macrophages and express a number of non-canonical osteoclast genes that are associated with structural and functional bone phenotypes when deleted in mice. Furthermore, genetic variation in human orthologs of osteomorph genes causes monogenic skeletal disorders and associates with bone mineral density, a polygenetic skeletal trait. Thus, osteoclasts recycle via osteomorphs, a cell type involved in the regulation of bone resorption that may be targeted for the treatment of skeletal diseases.

Journal article

Steinberg J, Southam L, Roumeliotis T, Clark MJ, Jayasuriya RL, Swift D, Shah KM, Butterfield NC, Brooks RA, McCaskie AW, Bassett JHD, Williams GR, Choudhary JS, Wilkinson JM, Zeggini Eet al., 2021, A molecular quantitative trait locus map for osteoarthritis, Nature Communications, Vol: 12, Pages: 1-11, ISSN: 2041-1723

Osteoarthritis causes pain and functional disability for over 500 million people worldwide. To develop disease-stratifying tools and modifying therapies, we need a better understanding of the molecular basis of the disease in relevant tissue and cell types. Here, we study primary cartilage and synovium from 115 patients with osteoarthritis to construct a deep molecular signature map of the disease. By integrating genetics with transcriptomics and proteomics, we discover molecular trait loci in each tissue type and omics level, identify likely effector genes for osteoarthritis-associated genetic signals and highlight high-value targets for drug development and repurposing. These findings provide insights into disease aetiopathology, and offer translational opportunities in response to the global clinical challenge of osteoarthritis.

Journal article

Bassett J, Williams GR, 2021, Accelerating functional gene discovery in osteoarthritis, Nature Communications, Vol: 12, Pages: 1-18, ISSN: 2041-1723

Osteoarthritis causes debilitating pain and disability, resulting in a considerablesocioeconomic burden, yet no drugs are available that prevent disease onset or progression.Here, we develop, validate and use rapid-throughput imaging techniques to identify abnormaljoint phenotypes in randomly selected mutant mice generated by the International KnockoutMouse Consortium. We identify 14 genes with functional involvement in osteoarthritispathogenesis, including the homeobox gene Pitx1, and functionally characterize 6 candidatehuman osteoarthritis genes in mouse models. We demonstrate sensitivity of the methods byidentifying age-related degenerative joint damage in wild-type mice. Finally, we phenotypepreviously generated mutant mice with an osteoarthritis-associated polymorphism in the Dio2gene by CRISPR/Cas9 genome editing and demonstrate a protective role in disease onsetwith public health implications. This expanding resource of mutant mice will acceleratefunctional gene discovery in osteoarthritis and offer drug discovery opportunities for thiscommon, incapacitating chronic disease.

Journal article

Winter EM, Ireland A, Butterfield NC, Haffner-Luntzer M, Horcajada M-N, Veldhuis-Vlug AG, Oei L, Colaianni G, Bonnet Net al., 2020, Pregnancy and lactation, a challenge for the skeleton, ENDOCRINE CONNECTIONS, Vol: 9, Pages: R143-R157, ISSN: 2049-3614

Journal article

Joustra SD, Roelfsema F, van Trotsenburg ASP, Schneider HJ, Kosilek RP, Kroon HM, Logan JG, Butterfield NC, Zhou X, Toufaily C, Bak B, Turgeon M-O, Brule E, Steyn FJ, Gurnell M, Koulouri O, Le Tissier P, Fontanaud P, Bassett JHD, Williams GR, Oostdijk W, Wit JM, Pereira AM, Biermasz NR, Bernard DJ, Schoenmakers Net al., 2020, Response to Letter to the Editor: "IGSF1 Deficiency Results in Human and Murine Somatotrope Neurosecretory Hyperfunction", JOURNAL OF CLINICAL ENDOCRINOLOGY & METABOLISM, Vol: 105, Pages: E2315-E2316, ISSN: 0021-972X

Journal article

Joustra SD, Roelfsema F, van Trotsenburg ASP, Schneider HJ, Kosilek RP, Kroon HM, Logan JG, Butterfield NC, Zhou X, Toufaily C, Bak B, Turgeon M-O, Brule E, Steyn FJ, Gurnell M, Koulouri O, Le Tissier P, Fontanaud P, Bassett JHD, Williams GR, Oostdijk W, Wit JM, Pereira AM, Biermasz NR, Bernard DJ, Schoenmakers Net al., 2020, IGSF1 Deficiency Results in Human and Murine Somatotrope Neurosecretory Hyperfunction, JOURNAL OF CLINICAL ENDOCRINOLOGY & METABOLISM, Vol: 105, Pages: E70-E84, ISSN: 0021-972X

Journal article

Leitch VD, Brassill MJ, Rahman S, Butterfield NC, Ma P, Logan JG, Boyde A, Evans H, Croucher PI, Batterham RL, Williams GR, Bassett JHDet al., 2019, PYY is a negative regulator of bone mass and strength, Bone, Vol: 127, Pages: 427-435, ISSN: 8756-3282

ObjectiveBone loss in anorexia nervosa and following bariatric surgery is associated with an elevated circulating concentration of the gastrointestinal, anorexigenic hormone, peptide YY (PYY). Selective deletion of the PYY receptor Y1R in osteoblasts or Y2R in the hypothalamus results in high bone mass, but deletion of PYY in mice has resulted in conflicting skeletal phenotypes leading to uncertainty regarding its role in the regulation of bone mass. As PYY analogs are under development for treatment of obesity, we aimed to clarify the relationship between PYY and bone mass.MethodsThe skeletal phenotype of Pyy knockout (KO) mice was investigated during growth (postnatal day P14) and adulthood (P70 and P186) using X-ray microradiography, micro-CT, back-scattered electron scanning electron microscopy (BSE-SEM), histomorphometry and biomechanical testing.ResultsBones from juvenile and Pyy KO mice were longer (P < 0.001), with decreased bone mineral content (P < 0.001). Whereas, bones from adult Pyy KO mice had increased bone mineral content (P < 0.05) with increased mineralisation of both cortical (P < 0.001) and trabecular (P < 0.001) compartments. Long bones from adult Pyy KO mice were stronger (maximum load P < 0.001), with increased stiffness (P < 0.01) and toughness (P < 0.05) compared to wild-type (WT) control mice despite increased cortical vascularity and porosity (P < 0.001). The increased bone mass and strength in Pyy KO mice resulted from increases in trabecular (P < 0.01) and cortical bone formation (P < 0.05).ConclusionsThese findings demonstrate that PYY acts as a negative regulator of osteoblastic bone formation, implicating increased PYY levels in the pathogenesis of bone loss during anorexia or following bariatric surgery.

Journal article

Beck-Cormier S, Lelliott CJ, Logan JG, Lafont DT, Leitch VD, Butterfield NC, Protheroe HJ, Croucher PI, Baldock PA, Gaultier-Lintia A, Nicolas G, Bon N, Sourice S, Guicheux J, Beck L, Williams GR, Bassett JHDet al., 2019, Slc20a2, encoding the phosphate transporter PiT2, is a novel genetic determinant of bone quality and strength, Journal of Bone and Mineral Research, Vol: 34, Pages: 1101-1114, ISSN: 1523-4681

Osteoporosis is characterized by low bone mineral density (BMD) and fragility fracture and affects over 200 million people worldwide. Bone quality describes the material properties that contribute to strength independently of BMD, and its quantitative analysis is a major priority in osteoporosis research. Tissue mineralization is a fundamental process requiring calcium and phosphate transporters. Here we identify impaired bone quality and strength in Slc20a2–/– mice lacking the phosphate transporter SLC20A2. Juveniles had abnormal endochondral and intramembranous ossification, decreased mineral accrual, and short stature. Adults exhibited only small reductions in bone mass and mineralization but a profound impairment of bone strength. Bone quality was severely impaired in Slc20a2–/– mice: yield load (–2.3 SD), maximum load (–1.7 SD), and stiffness (–2.7 SD) were all below values predicted from their bone mineral content as determined in a cohort of 320 wild‐type controls. These studies identify Slc20a2 as a physiological regulator of tissue mineralization and highlight its critical role in the determination of bone quality and strength.

Journal article

Freudenthal B, Shetty S, Butterfield NC, Logan JG, Han CR, Zhu X-G, Astapova I, Hollenberg AN, Cheng S-Y, Bassett JHD, Williams Get al., 2019, Genetic and pharmacological targeting of transcriptional repression in resistance to thyroid hormone alpha, Thyroid, Vol: 29, ISSN: 1050-7256

Background Thyroid hormones act in bone and cartilage via thyroid hormone receptor α (TRα). In the absence of T3, TRα interacts with co-repressors, including nuclear receptor co-repressor-1 (NCoR1), which recruit histone deacetylases (HDACs) and mediate transcriptional repression. Dominant-negative mutations of TRα cause resistance to thyroid hormone α (RTHα; OMIM 614450), characterized by excessive repression of T3 target genes leading to delayed skeletal development, growth retardation and bone dysplasia. Treatment with thyroxine has been of limited benefit even in mildly affected individuals and there is a need for new therapeutic strategies. We hypothesized that (i) the skeletal manifestations of RTHα are mediated by the persistent TRα/NCoR1/HDAC repressor complex containing mutant TRα, and (ii) treatment with the HDAC inhibitor suberoylanilide hydroxamic acid (SAHA) would ameliorate these manifestations. Methods We determined the skeletal phenotypes of (i) Thra1PV/+ mice, a well characterized model of RTHα, (ii) Ncor1ΔID/ΔID mice, which express an NCoR1 mutant that fails to interact with TRα, and (iii) Thra1PV/+Ncor1ΔID/ΔID double mutant adult mice. Wild-type, Thra1PV/+, Ncor1ΔID/ΔID, and Thra1PV/+Ncor1ΔID/ΔID double mutant mice were also treated with SAHA to determine whether HDAC inhibition results in amelioration of skeletal abnormalities. Results Thra1PV/+ mice had a severe skeletal dysplasia characterized by short stature, abnormal bone morphology and increased bone mineral content. Despite normal bone length, Ncor1ΔID/ΔID mice displayed increased cortical bone mass, mineralization and strength. Thra1PV/+Ncor1ΔID/ΔID double mutant mice displayed only a small improvement of skeletal abnormalities compared to Thra1PV/+ mice. Treatment with SAHA to inhibit histone deacetylation had no beneficial or detrimental effects on bo

Journal article

Butterfield NC, Logan JG, Waung J, Williams GR, Bassett JHDet al., 2019, Quantitative X-Ray Imaging of Mouse Bone by Faxitron., Methods Mol Biol, Vol: 1914, Pages: 559-569

This chapter describes the use of point projection digital microradiography for rapid imaging and quantitation of bone mineral content in mice.

Journal article

Morris JA, Kemp JP, Youlten SE, Laurent L, Logan JG, Chai RC, Vulpescu NA, Forgetta V, Kleinman A, Mohanty ST, Sergio CM, Quinn J, Nguyen-Yamamoto L, Luco A-L, Vijay J, Simon M-M, Pramatarova A, Medina-Gomez C, Trajanoska K, Ghirardello EJ, Butterfield NC, Curry KF, Leitch VD, Sparkes PC, Adoum A-T, Mannan NS, Komla-Ebri DSK, Pollard AS, Dewhurst HF, Hassall TAD, Beltejar M-JG, Agee M, Alipanahi B, Auton A, Bell RK, Bryc K, Elson SL, Fontanillas P, Furlotte NA, McCreight JC, Huber KE, Litterman NK, McIntyre MH, Mountain JL, Noblin ES, Northover CAM, Pitts SJ, Sathirapongsasuti JF, Sazonova OV, Shelton JF, Shringarpure S, Tian C, Tung JY, Vacic V, Wilson CH, Adams DJ, Vaillancourt SM, Kaptoge S, Baldock P, Cooper C, Reeve J, Ntzani EE, Evangelou E, Ohlsson C, Karasik D, Rivadeneira F, Kiel DP, Tobias JH, Gregson CL, Harvey NC, Grundberg E, Goltzman D, Adams DJ, Lelliott CJ, Hinds DA, Ackert-Bicknell CL, Hsu Y-H, Maurano MT, Croucher PI, Williams GR, Bassett JHD, Evans DM, Richards JBet al., 2019, An atlas of genetic influences on osteoporosis in humans and mice, Nature Genetics, Vol: 51, Pages: 258-266, ISSN: 1061-4036

Osteoporosis is a common aging-related disease diagnosed primarily using bone mineral density (BMD). We assessed genetic determinants of BMD as estimated by heel quantitative ultrasound in 426,824 individuals, identifying 518 genome-wide significant loci (301 novel), explaining 20% of its variance. We identified 13 bone fracture loci, all associated with estimated BMD (eBMD), in ~1.2 million individuals. We then identified target genes enriched for genes known to influence bone density and strength (maximum odds ratio (OR) = 58, P = 1 × 10−75) from cell-specific features, including chromatin conformation and accessible chromatin sites. We next performed rapid-throughput skeletal phenotyping of 126 knockout mice with disruptions in predicted target genes and found an increased abnormal skeletal phenotype frequency compared to 526 unselected lines (P < 0.0001). In-depth analysis of one gene, DAAM2, showed a disproportionate decrease in bone strength relative to mineralization. This genetic atlas provides evidence linking associated SNPs to causal genes, offers new insight into osteoporosis pathophysiology, and highlights opportunities for drug development.

Journal article

Jo S, Fonseca TL, Da Costa Bocco BM, Fernandes GW, McAninch EA, Bolin AP, Da Conceição RR, De Castro JPW, Ignacio DL, Egri P, Németh D, Fekete C, Bernardi MM, Leitch VD, Mannan NS, Curry KF, Butterfield NC, Bassett JHD, Williams GR, Gereben B, Ribeiro MO, Bianco ACet al., 2019, Type 2 deiodinase polymorphism causes ER stress and hypothyroidism in the brain, Journal of Clinical Investigation, Vol: 129, Pages: 230-245, ISSN: 0021-9738

Levothyroxine (LT4) is a form of thyroid hormone used to treat hypothyroidism. In the brain, T4 is converted to the active form T3 by the type 2 deiodinase (D2). Thus, it is intriguing that carriers of the Thr92Ala polymorphism in the D2 gene (DIO2) exhibit clinical improvement when liothyronine (LT3) is added to LT4 therapy. Here we report that D2 is a cargo protein in endoplasmic reticulum Golgi intermediary compartment (ERGIC) vesicles, recycling between ER and Golgi. The Thr92 to Ala substitution (Ala92-D2) caused ER stress and activated the unfolded protein response (UPR); Ala92-D2 accumulated in the trans-Golgi and generated less T3, all of which was restored by eliminating ER stress with the chemical chaperone 4-phenyl butyric acid (4-PBA). An Ala92-Dio2 polymorphism-carrying mouse exhibited UPR and hypothyroidism in distinct brain areas. The mouse refrained from physical activity, slept more and required additional time to memorize objects. Enhancing T3 signaling in the brain with LT3 improved cognition, whereas restoring proteostasis with 4-PBA eliminated the Ala92-Dio2 phenotype. In contrast, primary hypothyroidism intensified the Ala92-Dio2 phenotype, with only partial response to LT4 therapy. Disruption of cellular proteostasis and reduced Ala92-D2 activity may explain the failure of LT4 therapy in carriers of Thr92Ala-DIO2.

Journal article

Kemp JP, Morris JA, Medina-Gomez C, Forgetta V, Warrington NM, Youlten SE, Zheng J, Gregson CL, Grundberg E, Trajanoska K, Logan JG, Pollard AS, Sparkes PC, Ghirardello EJ, Allen R, Leitch VD, Butterfield NC, Komla-Ebri D, Adoum A-T, Curry KF, White JK, Kussy F, Greenlaw KM, Xu C, Harvey NC, Cooper C, Adams DJ, Greenwood CMT, Maurano MT, Kaptoge S, Rivadeneira F, Tobias JH, Croucher PI, Ackert-Bicknell CL, Bassett JHD, Williams GR, Richards JB, Evans DMet al., 2017, Identification of 153 new loci associated with heel bone mineral density and functional involvement of GPC6 in osteoporosis, Nature Genetics, Vol: 49, Pages: 1468-1475, ISSN: 1061-4036

Osteoporosis is a common disease diagnosed primarily by measurement of bone mineral density (BMD). We undertook a genome-wide association study (GWAS) in 142,487 individuals from the UK Biobank to identify loci associated with BMD as estimated by quantitative ultrasound of the heel. We identified 307 conditionally independent single-nucleotide polymorphisms (SNPs) that attained genome-wide significance at 203 loci, explaining approximately 12% of the phenotypic variance. These included 153 previously unreported loci, and several rare variants with large effect sizes. To investigate the underlying mechanisms, we undertook (1) bioinformatic, functional genomic annotation and human osteoblast expression studies; (2) gene-function prediction; (3) skeletal phenotyping of 120 knockout mice with deletions of genes adjacent to lead independent SNPs; and (4) analysis of gene expression in mouse osteoblasts, osteocytes and osteoclasts. The results implicate GPC6 as a novel determinant of BMD, and also identify abnormal skeletal phenotypes in knockout mice associated with a further 100 prioritized genes.

Journal article

Butterfield NC, Qian C, Logan MPO, 2017, Pitx1 determines characteristic hindlimb morphologies in cartilage micromass culture, PLOS ONE, Vol: 12, ISSN: 1932-6203

The shapes of homologous skeletal elements in the vertebrate forelimb and hindlimb are distinct, with each element exquisitely adapted to their divergent functions. Many of the signals and signalling pathways responsible for patterning the developing limb bud are common to both forelimb and hindlimb. How disparate morphologies are generated from common signalling inputs during limb development remains poorly understood. We show that, similar to what has been shown in the chick, characteristic differences in mouse forelimb and hindlimb cartilage morphology are maintained when chondrogenesis proceeds in vitro away from the endogenous limb bud environment. Chondrogenic nodules that form in high-density micromass cultures derived from forelimb and hindlimb buds are consistently different in size and shape. We described analytical tools we have developed to quantify these differences in nodule morphology and demonstrate that characteristic hindlimb nodule morphology is lost in the absence of the hindlimb-restricted limb modifier gene Pitx1. Furthermore, we show that ectopic expression of Pitx1 in the forelimb is sufficient to generate nodule patterns characteristic of the hindlimb. We also demonstrate that hindlimb cells are less adhesive to the tissue culture substrate and, within the limb environment, to the extracellular matrix and to each other. These results reveal autonomously programmed differences in forelimb and hindlimb cartilage precursors of the limb skeleton are controlled, at least in part, by Pitx1 and suggest this has an important role in generating distinct limb-type morphologies. Our results demonstrate that the micromass culture system is ideally suited to study cues governing morphogenesis of limb skeletal elements in a simple and experimentally tractable in vitro system that reflects in vivo potential.

Journal article

Sulaiman FA, Nishimoto S, Murphy GRF, Kucharska A, Butterfield NC, Newbury-Ecob R, Logan MPOet al., 2016, Tbx5 Buffers Inherent Left/Right Asymmetry Ensuring Symmetric Forelimb Formation, PLoS Genetics, Vol: 12, ISSN: 1553-7390

The forelimbs and hindlimbs of vertebrates are bilaterally symmetric. The mechanisms thatensure symmetric limb formation are unknown but they can be disrupted in disease. In HoltOramSyndrome (HOS), caused by mutations in TBX5, affected individuals have left-biasedupper/forelimb defects. We demonstrate a role for the transcription factor Tbx5 in ensuringthe symmetric formation of the left and right forelimb. In our mouse model, bilateral hypomorphiclevels of Tbx5 produces asymmetric forelimb defects that are consistently moresevere in the left limb than the right, phenocopying the left-biased limb defects seen in HOSpatients. In Tbx hypomorphic mutants maintained on an INV mutant background, with situsinversus, the laterality of defects is reversed. Our data demonstrate an early, inherent asymmetryin the left and right limb-forming regions and that threshold levels of Tbx5 are requiredto overcome this asymmetry to ensure symmetric forelimb formation.

Journal article

Ashe A, Butterfield NC, Town L, Courtney AD, Cooper AN, Ferguson C, Barry R, Olsson F, Liem KF, Parton RG, Wainwright BJ, Anderson KV, Whitelaw E, Wicking Cet al., 2012, Mutations in mouse <i>Ift144</i> model the craniofacial, limb and rib defects in skeletal ciliopathies, HUMAN MOLECULAR GENETICS, Vol: 21, Pages: 1808-1823, ISSN: 0964-6906

Journal article

Bruce SJ, Butterfield NC, Metzis V, Town L, McGlinn E, Wicking Cet al., 2010, Inactivation of <i>Patched1</i> in the Mouse Limb Has Novel Inhibitory Effects on the Chondrogenic Program, JOURNAL OF BIOLOGICAL CHEMISTRY, Vol: 285, Pages: 27967-27981

Journal article

Butterfield NC, McGlinn E, Wicking C, 2010, THE MOLECULAR REGULATION OF VERTEBRATE LIMB PATTERNING, ORGANOGENESIS IN DEVELOPMENT, Vol: 90, Pages: 319-341, ISSN: 0070-2153

Journal article

Town L, McGlinn E, Fiorenza S, Metzis V, Butterfield NC, Richman JM, Wicking Cet al., 2009, The Metalloendopeptidase Gene <i>Pitrm1</i> Is Regulated by Hedgehog Signaling in the Developing Mouse Limb and Is Expressed in Muscle Progenitors, DEVELOPMENTAL DYNAMICS, Vol: 238, Pages: 3175-3184, ISSN: 1058-8388

Journal article

Butterfield NC, Metzis V, McGlinn E, Bruce SJ, Wainwright BJ, Wicking Cet al., 2009, Patched 1 is a crucial determinant of asymmetry and digit number in the vertebrate limb, DEVELOPMENT, Vol: 136, Pages: 3515-3524, ISSN: 0950-1991

Journal article

McGlinn E, Richman JM, Metzis V, Town L, Butterfield NC, Wainwright BJ, Wicking Cet al., 2008, Expression of the NET family member <i>Zfp503</i> is regulated by hedgehog and BMP signaling in the limb, DEVELOPMENTAL DYNAMICS, Vol: 237, Pages: 1172-1182, ISSN: 1058-8388

Journal article

Ashe A, Morgan DK, Whitelaw NC, Bruxner TJ, Vickaryous NK, Cox LL, Butterfield NC, Wicking C, Blewitt ME, Wilkins SJ, Anderson GJ, Cox TC, Whitelaw Eet al., 2008, A genome-wide screen for modifiers of transgene variegation identifies genes with critical roles in development, GENOME BIOLOGY, Vol: 9, ISSN: 1474-760X

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Bennetts JS, Fowles LF, Butterfield NC, Berkman JL, Teasdale RD, Simpson F, Wicking Cet al., 2006, Identification and analysis of novel genes expressed in the mouse embryonic facial primordia, FRONTIERS IN BIOSCIENCE-LANDMARK, Vol: 11, Pages: 2631-2646, ISSN: 1093-9946

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SIMPSON F, LAMMERTSVANBUEREN K, BUTTERFIELD N, BENNETTS J, BOWLES J, ADOLPHE C, SIMMS L, YOUNG J, WALSH M, LEGGETT Bet al., 2006, The PCNA-associated factor KIAA0101/p15 binds the potential tumor suppressor product p33ING1b, Experimental Cell Research, Vol: 312, Pages: 73-85, ISSN: 0014-4827

Journal article

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