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Clifford J. Tabin

Aysu Uygur, John Young, Tyler R Huycke, Mervenaz Koska, James Briscoe, Clifford J Tabin
Anatomical proportions are robustly maintained in individuals that vary enormously in size, both within a species and between members of related taxa. However, the mechanisms underlying scaling are still poorly understood. We have examined this phenomenon in the context of the patterning of the ventral neural tube in response to a gradient of the morphogen Sonic hedgehog (SHH) in the chick and zebra finch, two species that differ in size during the time of neural tube patterning. We find that scaling is achieved, at least in part, by altering the sensitivity of the target cells to SHH and appears to be achieved by modulating the ratio of the repressive and activating transcriptional regulators, GLI2 and GLI3...
April 18, 2016: Developmental Cell
Jessica A Lehoczky, Clifford J Tabin
The tips of the digits of some mammals, including human infants and mice, are capable of complete regeneration after injury. This process is reliant on the presence of the overlaying nail organ and is mediated by a proliferative blastema. Epithelial Wnt/β-catenin signaling has been shown to be necessary for mouse digit tip regeneration. Here, we report on Lgr5 and Lgr6 (leucine-rich repeat-containing G protein-coupled receptor 5 and 6), two important agonists of the Wnt pathway that are known to be markers of several epithelial stem cell populations...
October 27, 2015: Proceedings of the National Academy of Sciences of the United States of America
Talia Y Moore, Chris L Organ, Scott V Edwards, Andrew A Biewener, Clifford J Tabin, Farish A Jenkins, Kimberly L Cooper
Recent rapid advances in experimental biology have expanded the opportunity for interdisciplinary investigations of the evolution of form and function in non-traditional model species. However, historical divisions of philosophy and methodology between evolutionary/organismal biologists and developmental geneticists often preclude an effective merging of disciplines. In an effort to overcome these divisions, we take advantage of the extraordinary morphological diversity of the rodent superfamily Dipodoidea, including the bipedal jerboas, to experimentally study the developmental mechanisms and biomechanical performance of a remarkably divergent limb structure...
November 2, 2015: Current Biology: CB
Siew Fen Lisa Wong, Vikram Agarwal, Jennifer H Mansfield, Nicolas Denans, Matthew G Schwartz, Haydn M Prosser, Olivier Pourquié, David P Bartel, Clifford J Tabin, Edwina McGlinn
The Hox genes play a central role in patterning the embryonic anterior-to-posterior axis. An important function of Hox activity in vertebrates is the specification of different vertebral morphologies, with an additional role in axis elongation emerging. The miR-196 family of microRNAs (miRNAs) are predicted to extensively target Hox 3' UTRs, although the full extent to which miR-196 regulates Hox expression dynamics and influences mammalian development remains to be elucidated. Here we used an extensive allelic series of mouse knockouts to show that the miR-196 family of miRNAs is essential both for properly patterning vertebral identity at different axial levels and for modulating the total number of vertebrae...
September 1, 2015: Proceedings of the National Academy of Sciences of the United States of America
Yana G Kamberov, Elinor K Karlsson, Gerda L Kamberova, Daniel E Lieberman, Pardis C Sabeti, Bruce A Morgan, Clifford J Tabin
Among the unique features of humans, one of the most salient is the ability to effectively cool the body during extreme prolonged activity through the evapotranspiration of water on the skin's surface. The evolution of this novel physiological ability required a dramatic increase in the density and distribution of eccrine sweat glands relative to other mammals and a concomitant reduction of body hair cover. Elucidation of the genetic underpinnings for these adaptive changes is confounded by a lack of knowledge about how eccrine gland fate and density are specified during development...
August 11, 2015: Proceedings of the National Academy of Sciences of the United States of America
Ariel C Aspiras, Nicolas Rohner, Brian Martineau, Richard L Borowsky, Clifford J Tabin
Despite recent advances in the understanding of morphological evolution, the genetic underpinnings of behavioral and physiological evolution remain largely unknown. Here, we study the metabolic changes that evolved in independently derived populations of the Mexican cavefish, Astyanax mexicanus. A hallmark of cave environments is scarcity of food. Cavefish populations rely almost entirely on sporadic food input from outside of the caves. To survive under these conditions, cavefish have evolved a range of adaptations, including starvation resistance and binge eating when food becomes available...
August 4, 2015: Proceedings of the National Academy of Sciences of the United States of America
Amy E Shyer, Tyler R Huycke, ChangHee Lee, L Mahadevan, Clifford J Tabin
We address the mechanism by which adult intestinal stem cells (ISCs) become localized to the base of each villus during embryonic development. We find that, early in gut development, proliferating progenitors expressing ISC markers are evenly distributed throughout the epithelium, in both the chick and mouse. However, as the villi form, the putative stem cells become restricted to the base of the villi. This shift in the localization is driven by mechanically influenced reciprocal signaling between the epithelium and underlying mesenchyme...
April 23, 2015: Cell
Patrick Tschopp, Emma Sherratt, Thomas J Sanger, Anna C Groner, Ariel C Aspiras, Jimmy K Hu, Olivier Pourquié, Jérôme Gros, Clifford J Tabin
The move of vertebrates to a terrestrial lifestyle required major adaptations in their locomotory apparatus and reproductive organs. While the fin-to-limb transition has received considerable attention, little is known about the developmental and evolutionary origins of external genitalia. Similarities in gene expression have been interpreted as a potential evolutionary link between the limb and genitals; however, no underlying developmental mechanism has been identified. We re-examined this question using micro-computed tomography, lineage tracing in three amniote clades, and RNA-sequencing-based transcriptional profiling...
December 18, 2014: Nature
Kimberly L Cooper, Karen E Sears, Aysu Uygur, Jennifer Maier, Karl-Stephan Baczkowski, Margaret Brosnahan, Doug Antczak, Julian A Skidmore, Clifford J Tabin
A reduction in the number of digits has evolved many times in tetrapods, particularly in cursorial mammals that travel over deserts and plains, yet the underlying developmental mechanisms have remained elusive. Here we show that digit loss can occur both during early limb patterning and at later post-patterning stages of chondrogenesis. In the 'odd-toed' jerboa (Dipus sagitta) and horse and the 'even-toed' camel, extensive cell death sculpts the tissue around the remaining toes. In contrast, digit loss in the pig is orchestrated by earlier limb patterning mechanisms including downregulation of Ptch1 expression but no increase in cell death...
July 3, 2014: Nature
Jerome Gros, Clifford J Tabin
Vertebrate limbs first emerge as small buds at specific locations along the trunk. Although a fair amount is known about the molecular regulation of limb initiation and outgrowth, the cellular events underlying these processes have remained less clear. We show that the mesenchymal limb progenitors arise through localized epithelial-to-mesenchymal transition (EMT) of the coelomic epithelium specifically within the presumptive limb fields. This EMT is regulated at least in part by Tbx5 and Fgf10, two genes known to control limb initiation...
March 14, 2014: Science
Nicolas Rohner, Dan F Jarosz, Johanna E Kowalko, Masato Yoshizawa, William R Jeffery, Richard L Borowsky, Susan Lindquist, Clifford J Tabin
In the process of morphological evolution, the extent to which cryptic, preexisting variation provides a substrate for natural selection has been controversial. We provide evidence that heat shock protein 90 (HSP90) phenotypically masks standing eye-size variation in surface populations of the cavefish Astyanax mexicanus. This variation is exposed by HSP90 inhibition and can be selected for, ultimately yielding a reduced-eye phenotype even in the presence of full HSP90 activity. Raising surface fish under conditions found in caves taxes the HSP90 system, unmasking the same phenotypic variation as does direct inhibition of HSP90...
December 13, 2013: Science
Kathryn D Kavanagh, Oren Shoval, Benjamin B Winslow, Uri Alon, Brian P Leary, Akinori Kan, Clifford J Tabin
Evolutionary theory has long argued that the entrenched rules of development constrain the range of variations in a given form, but few empirical examples are known. Here we provide evidence for a very deeply conserved skeletal module constraining the morphology of the phalanges within a digit. We measured the sizes of phalanges within populations of two bird species and found that successive phalanges within a digit exhibit predictable relative proportions, whether those phalanges are nearly equal in size or exhibit a more striking gradient in size from large to small...
November 5, 2013: Proceedings of the National Academy of Sciences of the United States of America
Johanna E Kowalko, Nicolas Rohner, Tess A Linden, Santiago B Rompani, Wesley C Warren, Richard Borowsky, Clifford J Tabin, William R Jeffery, Masato Yoshizawa
When an organism colonizes a new environment, it needs to adapt both morphologically and behaviorally to survive and thrive. Although recent progress has been made in understanding the genetic architecture underlying morphological evolution, behavioral evolution is poorly understood. Here, we use the Mexican cavefish, Astyanax mexicanus, to study the genetic basis for convergent evolution of feeding posture. When river-dwelling surface fish became entrapped in the caves, they were confronted with dramatic changes in the availability and type of food source and in their ability to perceive it...
October 15, 2013: Proceedings of the National Academy of Sciences of the United States of America
Johanna E Kowalko, Nicolas Rohner, Santiago B Rompani, Brant K Peterson, Tess A Linden, Masato Yoshizawa, Emily H Kay, Jesse Weber, Hopi E Hoekstra, William R Jeffery, Richard Borowsky, Clifford J Tabin
BACKGROUND: Surface populations of Astyanax mexicanus, living in rivers like their common ancestors, school, while several, independently derived cave populations of the same species have lost schooling behavior. RESULTS: We quantify schooling behavior in individual A. mexicanus and identify quantitative trait loci (QTL) for this trait. We find that the evolutionary modulation of schooling has both vision-dependent and -independent components. We also quantify differences in the lateral line and vision between cavefish and surface fish and relate these differences to the evolutionary loss of schooling behavior...
October 7, 2013: Current Biology: CB
Amy E Shyer, Tuomas Tallinen, Nandan L Nerurkar, Zhiyan Wei, Eun Seok Gil, David L Kaplan, Clifford J Tabin, L Mahadevan
The villi of the human and chick gut are formed in similar stepwise progressions, wherein the mesenchyme and attached epithelium first fold into longitudinal ridges, then a zigzag pattern, and lastly individual villi. We find that these steps of villification depend on the sequential differentiation of the distinct smooth muscle layers of the gut, which restrict the expansion of the growing endoderm and mesenchyme, generating compressive stresses that lead to their buckling and folding. A quantitative computational model, incorporating measured properties of the developing gut, recapitulates the morphological patterns seen during villification in a variety of species...
October 11, 2013: Science
Alan R Rodrigues, Clifford J Tabin
No abstract text is available yet for this article.
June 7, 2013: Science
Chris T Amemiya, Jessica Alföldi, Alison P Lee, Shaohua Fan, Hervé Philippe, Iain Maccallum, Ingo Braasch, Tereza Manousaki, Igor Schneider, Nicolas Rohner, Chris Organ, Domitille Chalopin, Jeramiah J Smith, Mark Robinson, Rosemary A Dorrington, Marco Gerdol, Bronwen Aken, Maria Assunta Biscotti, Marco Barucca, Denis Baurain, Aaron M Berlin, Gregory L Blatch, Francesco Buonocore, Thorsten Burmester, Michael S Campbell, Adriana Canapa, John P Cannon, Alan Christoffels, Gianluca De Moro, Adrienne L Edkins, Lin Fan, Anna Maria Fausto, Nathalie Feiner, Mariko Forconi, Junaid Gamieldien, Sante Gnerre, Andreas Gnirke, Jared V Goldstone, Wilfried Haerty, Mark E Hahn, Uljana Hesse, Steve Hoffmann, Jeremy Johnson, Sibel I Karchner, Shigehiro Kuraku, Marcia Lara, Joshua Z Levin, Gary W Litman, Evan Mauceli, Tsutomu Miyake, M Gail Mueller, David R Nelson, Anne Nitsche, Ettore Olmo, Tatsuya Ota, Alberto Pallavicini, Sumir Panji, Barbara Picone, Chris P Ponting, Sonja J Prohaska, Dariusz Przybylski, Nil Ratan Saha, Vydianathan Ravi, Filipe J Ribeiro, Tatjana Sauka-Spengler, Giuseppe Scapigliati, Stephen M J Searle, Ted Sharpe, Oleg Simakov, Peter F Stadler, John J Stegeman, Kenta Sumiyama, Diana Tabbaa, Hakim Tafer, Jason Turner-Maier, Peter van Heusden, Simon White, Louise Williams, Mark Yandell, Henner Brinkmann, Jean-Nicolas Volff, Clifford J Tabin, Neil Shubin, Manfred Schartl, David B Jaffe, John H Postlethwait, Byrappa Venkatesh, Federica Di Palma, Eric S Lander, Axel Meyer, Kerstin Lindblad-Toh
The discovery of a living coelacanth specimen in 1938 was remarkable, as this lineage of lobe-finned fish was thought to have become extinct 70 million years ago. The modern coelacanth looks remarkably similar to many of its ancient relatives, and its evolutionary proximity to our own fish ancestors provides a glimpse of the fish that first walked on land. Here we report the genome sequence of the African coelacanth, Latimeria chalumnae. Through a phylogenomic analysis, we conclude that the lungfish, and not the coelacanth, is the closest living relative of tetrapods...
April 18, 2013: Nature
Kimberly L Cooper, Seungeun Oh, Yongjin Sung, Ramachandra R Dasari, Marc W Kirschner, Clifford J Tabin
The wide diversity of skeletal proportions in mammals is evident upon a survey of any natural history museum's collections and allows us to distinguish between species even when reduced to their calcified components. Similarly, each individual is comprised of a variety of bones of differing lengths. The largest contribution to the lengthening of a skeletal element, and to the differential elongation of elements, comes from a dramatic increase in the volume of hypertrophic chondrocytes in the growth plate as they undergo terminal differentiation...
March 21, 2013: Nature
Akinori Kan, Clifford J Tabin
Joints form within the developing skeleton through the segmentation and cavitation of initially continuous cartilage condensations. However, the molecular pathways controlling joint formation largely remain to be clarified. In particular, while several critical secreted signals have been identified, no transcription factors have yet been described as acting in the early stages of joint formation. Working upstream of the early joint marker Wnt9a, we found that the transcription factor c-Jun plays a pivotal role in specifying joint cell fates...
March 1, 2013: Genes & Development
Jeramiah J Smith, Shigehiro Kuraku, Carson Holt, Tatjana Sauka-Spengler, Ning Jiang, Michael S Campbell, Mark D Yandell, Tereza Manousaki, Axel Meyer, Ona E Bloom, Jennifer R Morgan, Joseph D Buxbaum, Ravi Sachidanandam, Carrie Sims, Alexander S Garruss, Malcolm Cook, Robb Krumlauf, Leanne M Wiedemann, Stacia A Sower, Wayne A Decatur, Jeffrey A Hall, Chris T Amemiya, Nil R Saha, Katherine M Buckley, Jonathan P Rast, Sabyasachi Das, Masayuki Hirano, Nathanael McCurley, Peng Guo, Nicolas Rohner, Clifford J Tabin, Paul Piccinelli, Greg Elgar, Magali Ruffier, Bronwen L Aken, Stephen M J Searle, Matthieu Muffato, Miguel Pignatelli, Javier Herrero, Matthew Jones, C Titus Brown, Yu-Wen Chung-Davidson, Kaben G Nanlohy, Scot V Libants, Chu-Yin Yeh, David W McCauley, James A Langeland, Zeev Pancer, Bernd Fritzsch, Pieter J de Jong, Baoli Zhu, Lucinda L Fulton, Brenda Theising, Paul Flicek, Marianne E Bronner, Wesley C Warren, Sandra W Clifton, Richard K Wilson, Weiming Li
Lampreys are representatives of an ancient vertebrate lineage that diverged from our own ∼500 million years ago. By virtue of this deeply shared ancestry, the sea lamprey (P. marinus) genome is uniquely poised to provide insight into the ancestry of vertebrate genomes and the underlying principles of vertebrate biology. Here, we present the first lamprey whole-genome sequence and assembly. We note challenges faced owing to its high content of repetitive elements and GC bases, as well as the absence of broad-scale sequence information from closely related species...
April 2013: Nature Genetics
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