A new Adamts9 conditional mouse allele identifies its non-redundant role in interdigital web regression

Genesis

Volumn 52, Issue 7, 2014, Pages 702-712

  Dubail, Johanne ^a   Aramaki Hattori, Noriko ^a   Bader, Hannah L ^a   Nelson, Courtney M ^a   Katebi, Negin ^b   Matuska, Brittany ^a   Olsen, Bjorn R ^b   Apte, Suneel S ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

A disintegrin like and metalloprotease domain with thrombospondin type 1 motifs 9; Apoptosis; Cleft palate; Floxed; Interdigital web; Melanoblast; Prx1 Cre; Soft tissue syndactyly

Indexed keywords

ADAMTS9 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; ADAM PROTEIN; ADAMTS9 PROTEIN, MOUSE;

ADAMTS9 GENE; ADULT; ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOLOGICAL FUNCTIONS; CLEFT PALATE; DISEASE SEVERITY; EMBRYO DEATH; EMBRYO DEVELOPMENT; EMBRYONIC STRUCTURES; ENZYME ACTIVE SITE; EXON; GASTRULATION; GENE; GENE DELETION; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; GENOTYPE; GERM LINE; HAPLOINSUFFICIENCY; HEMIZYGOSITY; LETHALITY; LOXP SITE; MALE; MESODERM; NONHUMAN; NULL ALLELE; OUTCOME ASSESSMENT; PENETRANCE; PHENOTYPE; PRIORITY JOURNAL; REGRESSION ANALYSIS; SOFT TISSUE SYNDACTYLY; SPOTTING; SYNDACTYLY; ANIMAL; C57BL MOUSE; EMBRYOLOGY; GENETICS; LIMB; METABOLISM; MOUSE;

ADAM PROTEINS; ALLELES; ANIMALS; EXONS; EXTREMITIES; MESODERM; MICE; MICE, INBRED C57BL; PHENOTYPE; SYNDACTYLY;

EID: 84904285713     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.22784     Document Type: Article

References (31)

1. Apte SS. 2009. A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: Functions and mechanisms. J Biol Chem 284:31493-31497.
2. Blelloch R, Anna-Arriola SS, Gao D, Li Y, Hodgkin J, Kimble J. 1999. The gon-1 gene is required for gonadal morphogenesis in Caenorhabditis elegans. Dev Biol 216:382-393.
3. Chaemsaithong P, Madan I, Romero R, Than NG, Tarca AL, Draghici S, Bhatti G, Yeo L, Mazor M, Kim CJ, Hassan SS, Chaiworapongsa T. 2013. Characterization of the myometrial transcriptome in women with an arrest of dilatation during labor. J Perinat Med 41:665-681.
4. Clark ME, Kelner GS, Turbeville LA, Boyer A, Arden KC, Maki RA. 2000. ADAMTS9, a novel member of the ADAM-TS/metallospondin gene family. Genomics 67:343-350.
5. Du W, Wang S, Zhou Q, Li X, Chu J, Chang Z, Tao Q, Ng EK, Fang J, Sung JJ, Yu J. 2013. ADAMTS9 is a functional tumor suppressor through inhibiting AKT/mTOR pathway and associated with poor survival in gastric cancer. Oncogene 32:3319-3328.
6. Enomoto H, Nelson C, Somerville, RPT, Mielke K, Dixon L, Powell K, Apte SS. 2010. Cooperation of two ADAMTS metalloproteases in closure of the mouse palate identifies a requirement for versican proteolysis in regulating palatal mesenchyme proliferation. Development 137:4029-4038.
7. Heid IM, Jackson AU, Randall JC, Winkler TW, Qi L, Steinthorsdottir V, Thorleifsson G, Zillikens MC, Speliotes EK, Magi R, Workalemahu T, White CC, Bouatia-Naji N, Harris TB, Berndt SI, Ingelsson E, Willer CJ, Weedon MN, Luan J, Vedantam S, Esko T, Kilpelainen TO, Kutalik Z, Li S, Monda KL, Dixon AL, Holmes CC, Kaplan LM, Liang L, Min JL, Moffatt MF, Molony C, Nicholson G, Schadt EE, Zondervan KT, Feitosa MF, Ferreira T, Allen HL, Weyant RJ, Wheeler E, Wood AR, Estrada K, Goddard ME, Lettre G, Mangino M, Nyholt DR, Purcell S, Smith AV, Visscher PM, Yang J, McCarroll SA, Nemesh J, Voight BF, Absher D, Amin N, Aspelund T, Coin L, Glazer NL, Hayward C, Heard-Costa NL, Hottenga JJ, Johansson A, Johnson T, Kaakinen M, Kapur K, Ketkar S, Knowles JW, Kraft P, Kraja AT, Lamina C, Leitzmann MF, McKnight B, Morris AP, Ong KK, Perry JR, Peters MJ, Polasek O, Prokopenko I, Rayner NW, Ripatti S, Rivadeneira F, Robertson NR, Sanna S, Sovio U, Surakka I, Teumer A, van Wingerden S, Vitart V, Zhao JH, Cavalcanti-Proenca C, Chines PS, Fisher E, Kulzer JR, Lecoeur C, Narisu N, Sandholt C, Scott LJ, Silander K, Stark K, Tammesoo ML, Teslovich TM, Timpson NJ, Watanabe RM, Welch R, Chasman DI, Cooper MN, Jansson JO, Kettunen J, Lawrence RW, Pellikka N, Perola M, Vandenput L, Alavere H, Almgren P, Atwood LD, Bennett AJ, Biffar R, Bonnycastle LL, Bornstein SR, Buchanan TA, Campbell H, Day IN, Dei M, Dorr M, Elliott P, Erdos MR, Eriksson JG, Freimer NB, Fu M, Gaget S, Geus EJ, Gjesing AP, Grallert H, Grassler J, Groves CJ, Guiducci C, Hartikainen AL, Hassanali N, Havulinna AS, Herzig KH, Hicks AA, Hui J, Igl W, Jousilahti P, Jula A, Kajantie E, Kinnunen L, Kolcic I, Koskinen S, Kovacs P, Kroemer HK, Krzelj V, Kuusisto J, Kvaloy K, Laitinen J, Lantieri O, Lathrop GM, Lokki ML, Luben RN, Ludwig B, McArdle WL, McCarthy A, Morken MA, Nelis M, Neville MJ, Pare G, Parker AN, Peden JF, Pichler I, Pietilainen KH, Platou CG, Pouta A, Ridderstrale M, Samani NJ, Saramies J, Sinisalo J, Smit JH, Strawbridge RJ, Stringham HM, Swift AJ, Teder-Laving M, Thomson B, Usala G, van Meurs JB, van Ommen GJ, Vatin V, Volpato CB, Wallaschofski H, Walters GB, Widen E, Wild SH, Willemsen G, Witte DR, Zgaga L, Zitting P, Beilby JP, James AL, Kahonen M, Lehtimaki T, Nieminen MS, Ohlsson C, Palmer LJ, Raitakari O, Ridker PM, Stumvoll M, Tonjes A, Viikari J, Balkau B, Ben-Shlomo Y, Bergman RN, Boeing H, Smith GD, Ebrahim S, Froguel P, Hansen T, Hengstenberg C, Hveem K, Isomaa B, Jorgensen T, Karpe F, Khaw KT, Laakso M, Lawlor DA, Marre M, Meitinger T, Metspalu A, Midthjell K, Pedersen O, Salomaa V, Schwarz PE, Tuomi T, Tuomilehto J, Valle TT, Wareham NJ, Arnold AM, Beckmann JS, Bergmann S, Boerwinkle E, Boomsma DI, Caulfield MJ, Collins FS, Eiriksdottir G, Gudnason V, Gyllensten U, Hamsten A, Hattersley AT, Hofman A, Hu FB, Illig T, Iribarren C, Jarvelin MR, Kao WH, Kaprio J, Launer LJ, Munroe PB, Oostra B, Penninx BW, Pramstaller PP, Psaty BM, Quertermous T, Rissanen A, Rudan I, Shuldiner AR, Soranzo N, Spector TD, Syvanen AC, Uda M, Uitterlinden A, Volzke H, Vollenweider P, Wilson JF, Witteman JC, Wright AF, Abecasis GR, Boehnke M, Borecki IB, Deloukas P, Frayling TM, Groop LC, Haritunians T, Hunter DJ, Kaplan RC, North KE, O'Connell JR, Peltonen L, Schlessinger D, Strachan DP, Hirschhorn JN, Assimes TL, Wichmann HE, Thorsteinsdottir U, van Duijn CM, Stefansson K, Cupples LA, Loos RJ, Barroso I, McCarthy MI, Fox CS, Mohlke KL, Lindgren CM. 2010. Meta-analysis identifies 13 new loci associated with waist-hip ratio and reveals sexual dimorphism in the genetic basis of fat distribution. Nat Genet 42:949-960.
8. Helisalmi S, Immonen I, Losonczy G, Resch MD, Benedek S, Balogh I, Papp A, Berta A, Uusitupa M, Hiltunen M, Kaarniranta K. ADAMTS9 locus associates with increased risk of wet AMD. Acta Ophthalmol, 2014 Jan 16. doi: 10.1111/aos.12341. [Epub ahead of print].
9. Huang X, Hao C, Shen X, Zhang Y, Liu X. 2013. RUNX2, GPX3 and PTX3 gene expression profiling in cumulus cells are reflective oocyte/embryo competence and potentially reliable predictors of embryo developmental competence in PCOS patients. Reprod Biol Endocrinol 11:109.
10. Huxley-Jones J, Apte SS, Robertson DL, Boot-Handford RP. 2005. The characterisation of six ADAMTS proteases in the basal chordate Ciona intestinalis provides new insights into the vertebrate ADAMTS family. Int J Biochem Cell Biol 37:1838-1845.
11. Ismat A, Cheshire AM, Andrew DJ. 2013. The secreted AdamTS-A metalloprotease is required for collective cell migration. Development 140:1981-1993.
12. Jungers KA, Le Goff C, Somerville RP, Apte SS. 2005. Adamts9 is widely expressed during mouse embryo development. Gene Expr Patterns 5:609-617.
13. Kaufman MH. 1992. The atlas of mouse development, 1st ed. London: Academic Press.
14. Kern CB, Wessels A, McGarity J, Dixon LJ, Alston E, Argraves WS, Geeting D, Nelson CM, Menick DR, Apte SS. 2010. Reduced versican cleavage due to Adamts9 haploinsufficiency is associated with cardiac and aortic anomalies. Matrix Biol 29:304-316.
15. Koo BH, Coe DM, Dixon LJ, Somerville RP, Nelson CM, Wang LW, Young ME, Lindner DJ, Apte SS. 2010. ADAMTS9 is a cell-autonomously acting, anti-angiogenic metalloprotease expressed by microvascular endothelial cells. Am J Pathol 176:1494-1504.
16. Lewandoski M. 2007. Analysis of mouse development with conditional mutagenesis. Handb Exp Pharmacol 178:235-262.
17. Llamazares M, Cal S, Quesada V, Lopez-Otin C. 2003. Identification and characterization of ADAMTS-20 defines a novel subfamily of metalloproteinases-disintegrins with multiple thrombospondin-1 repeats and a unique GON domain. J Biol Chem 278:13382-13389.
18. Lo PH, Lung HL, Cheung AK, Apte SS, Chan KW, Kwong FM, Ko JM, Cheng Y, Law S, Srivastava G, Zabarovsky ER, Tsao SW, Tang JC, Stanbridge EJ, Lung ML. 2010. Extracellular protease ADAMTS9 suppresses esophageal and nasopharyngeal carcinoma tumor formation by inhibiting angiogenesis. Cancer Res 70:5567-5576.
19. Logan M, Martin JF, Nagy A, Lobe C, Olson EN, Tabin CJ. 2002. Expression of Cre recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33:77-80.
20. Lung HL, Lo PH, Xie D, Apte SS, Cheung AK, Cheng Y, Law EW, Chua D, Zeng YX, Tsao SW, Stanbridge EJ, Lung ML. 2008. Characterization of a novel epigenetically-silenced, growth-suppressive gene, ADAMTS9, and its association with lymph node metastases in nasopharyngeal carcinoma. Int J Cancer 123:401-408.
21. McCulloch DR, Nelson CM, Dixon LJ, Silver DL, Wylie JD, Lindner V, Sasaki T, Cooley MA, Argraves WS, Apte SS. 2009. ADAMTS metalloproteases generate active versican fragments that regulate interdigital web regression. Dev Cell 17:687-698.
22. Nandadasa S, Foulcer S, Apte SS. The multiple, complex roles of versican and its proteolytic turnover by ADAMTS proteases during embryogenesis. Matrix Biol, 2014 Jan 18. pii: S0945-053X(14)00006-7. doi: 10.1016/j.matbio.2014.01.005. [Epub ahead of print]
23. Pyun JA, Kim S, Cho NH, Koh I, Lee JY, Shin C, Kwack K. 2014. Genome-wide association studies and epistasis analyses of candidate genes related to age at menarche and age at natural menopause in a Korean population. Menopause 21:522-529. doi: 10.1097/GME.0b013e3182a433f7.
24. Rao C, Foernzler D, Loftus SK, Liu S, McPherson JD, Jungers KA, Apte SS, Pavan WJ, Beier DR. 2003. A defect in a novel ADAMTS family member is the cause of the belted white-spotting mutation. Development 130:4665-4672.
25. Rodriguez CI, Buchholz F, Galloway J, Sequerra R, Kasper J, Ayala R, Stewart AF, Dymecki SM. 2000. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat Genet 25:139-140.
26. Silver DL, Hou L, Somerville R, Young ME, Apte SS, Pavan WJ. 2008. The secreted metalloprotease ADAMTS20 is required for melanoblast survival. PLoS Genet 4:1-15.
27. Somerville RP, Longpre JM, Jungers KA, Engle JM, Ross M, Evanko S, Wight TN, Leduc R, Apte SS. 2003. Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1. J Biol Chem 278:9503-9513.
28. Thai SN, Iruela-Arispe ML. 2002. Expression of ADAMTS1 during murine development. Mech Dev 115:181-185.
29. Xiao R, Perveen Z, Paulsen D, Rouse R, Ambalavanan N, Kearney M, Penn AL. 2012. In utero exposure to second-hand smoke aggravates adult responses to irritants: Adult second-hand smoke. Am J Respir Cell Mol Biol 47:843-851.
30. Zeggini E, Scott LJ, Saxena R, Voight BF, Marchini JL, Hu T, de Bakker PI, Abecasis GR, Almgren P, Andersen G, Ardlie K, Bostrom KB, Bergman RN, Bonnycastle LL, Borch-Johnsen K, Burtt NP, Chen H, Chines PS, Daly MJ, Deodhar P, Ding CJ, Doney AS, Duren WL, Elliott KS, Erdos MR, Frayling TM, Freathy RM, Gianniny L, Grallert H, Grarup N, Groves CJ, Guiducci C, Hansen T, Herder C, Hitman GA, Hughes TE, Isomaa B, Jackson AU, Jorgensen T, Kong A, Kubalanza K, Kuruvilla FG, Kuusisto J, Langenberg C, Lango H, Lauritzen T, Li Y, Lindgren CM, Lyssenko V, Marvelle AF, Meisinger C, Midthjell K, Mohlke KL, Morken MA, Morris AD, Narisu N, Nilsson P, Owen KR, Palmer CN, Payne F, Perry JR, Pettersen E, Platou C, Prokopenko I, Qi L, Qin L, Rayner NW, Rees M, Roix JJ, Sandbaek A, Shields B, Sjogren M, Steinthorsdottir V, Stringham HM, Swift AJ, Thorleifsson G, Thorsteinsdottir U, Timpson NJ, Tuomi T, Tuomilehto J, Walker M, Watanabe RM, Weedon MN, Willer CJ, Illig T, Hveem K, Hu FB, Laakso M, Stefansson K, Pedersen O, Wareham NJ, Barroso I, Hattersley AT, Collins FS, Groop L, McCarthy MI, Boehnke M, Altshuler D. 2008. Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet 40:638-645.
31. Zhang C, Shao Y, Zhang W, Wu Q, Yang H, Zhong Q, Zhang J, Guan M, Yu B, Wan J. 2010. High-resolution melting analysis of ADAMTS9 methylation levels in gastric, colorectal, and pancreatic cancers. Cancer Genet Cytogenet 196:38-44.