Standard
The constrained maximal expression level owing to haploidy shapes gene content on the mammalian X chromosome. / Hurst, Laurence D.; Ghanbarian, Avazeh T.; Forrest, Alistair R R; Huminiecki, Lukasz; Rehli, Michael; Kenneth Baillie, J.; de Hoon, Michiel J L; Haberle, Vanja; Lassmann, Timo; Kulakovskiy, Ivan V.; Lizio, Marina; Itoh, Masayoshi; Andersson, Robin; Mungall, Christopher J.; Meehan, Terrence F.; Schmeier, Sebastian; Bertin, Nicolas; Jørgensen, Mette; Dimont, Emmanuel; Arner, Erik; Schmidl, Christian; Schaefer, Ulf; Medvedeva, Yulia A.; Plessy, Charles; Vitezic, Morana; Severin, Jessica; Semple, Colin A.; Ishizu, Yuri; Young, Robert S.; Francescatto, Margherita; Alam, Intikhab; Albanese, Davide; Altschuler, Gabriel M.; Arakawa, Takahiro; Archer, John A C; Arner, Peter; Babina, Magda; Baker, Sarah; Balwierz, Piotr J.; Beckhouse, Anthony G.; Pradhan, Swati Bhatt; Blake, Judith A.; Blumenthal, Antje; Bodega, Beatrice; Bonetti, Alessandro; Briggs, James; Brombacher, Frank; Maxwell Burroughs, A.; Califano, Andrea; Cannistraci, Carlo V.; Carbajo, Daniel; Chen, Yun; Chierici, Marco; Ciani, Yari; Clevers, Hans C.; Dalla, Emiliano; Davis, Carrie A.; Detmar, Michael; Diehl, Alexander D.; Dohi, Taeko; Drabløs, Finn; Edge, Albert S B; Edinger, Matthias; Ekwall, Karl; Endoh, Mitsuhiro; Enomoto, Hideki; Fagiolini, Michela; Fairbairn, Lynsey; Fang, Hai; Farach-Carson, Mary C.; Faulkner, Geoffrey J.; Favorov, Alexander V.; Fisher, Malcolm E.; Frith, Martin C.; Fujita, Rie; Fukuda, Shiro; Furlanello, Cesare; Furuno, Masaaki; Furusawa, Jun ichi; Geijtenbeek, Teunis B.; Gibson, Andrew; Gingeras, Thomas; Goldowitz, Daniel; Gough, Julian; Guhl, Sven; Guler, Reto; Gustincich, Stefano; Ha, Thomas J.; Hamaguchi, Masahide; Hara, Mitsuko; Harbers, Matthias; Harshbarger, Jayson; Hasegawa, Akira; Hasegawa, Yuki; Hashimoto, Takehiro; Herlyn, Meenhard; Hitchens, Kelly J.; Ho Sui, Shannan J.; Hofmann, Oliver M.; Hoof, Ilka; Hori, Fumi; Huminiecki, Lukasz; Iida, Kei; Ikawa, Tomokatsu; Jankovic, Boris R.; Jia, Hui; Joshi, Anagha; Jurman, Giuseppe; Kaczkowski, Bogumil; Kai, Chieko; Kaida, Kaoru; Kaiho, Ai; Kajiyama, Kazuhiro; Kanamori, Mutsumi Katayama; Kasianov, Artem S.; Kasukawa, Takeya; Katayama, Shintaro; Kato, Sachi; Kawaguchi, Shuji; Kawamoto, Hiroshi; Kawamura, Yuki I.; Kawashima, Tsugumi; Kempfle, Judith S.; Kenna, Tony J.; Kere, Juha; Khachigian, Levon M.; Kitamura, Toshio; Peter Klinken, S.; Knox, Alan J.; Kojima, Miki; Kojima, Soichi; Kondo, Naoto; Koseki, Haruhiko; Koyasu, Shigeo; Krampitz, Sarah; Kubosaki, Atsutaka; Kwon, Andrew T.; Laros, Jeroen F J; Lee, Weonju; Lennartsson, Andreas; Li, Kang; Lilje, Berit; Lipovich, Leonard; Mackay, Alan sim; Manabe, Riichiroh; Mar, Jessica C.; Marchand, Benoit; Mathelier, Anthony; Mejhert, Niklas; Meynert, Alison; Mizuno, Yosuke; de Lima Morais, David A.; Morikawa, Hiromasa; Morimoto, Mitsuru; Moro, Kazuyo; Motakis, Efthymios; Motohashi, Hozumi; Mummery, Christine L.; Murata, Mitsuyoshi; Nagao, Sayaka Sato; Nakachi, Yutaka; Nakahara, Fumio; Nakamura, Toshiyuki; Nakamura, Yukio; Nakazato, Kenichi; van Nimwegen, Erik; Ninomiya, Noriko; Nishiyori, Hiromi; Noma, Shohei; Nozaki, Tadasuke; Ogishima, Soichi; Ohkura, Naganari; Ohmiya, Hiroko; Ohno, Hiroshi; Ohshima, Mitsuhiro; Okada, Mariko Hatakeyama; Okazaki, Yasushi; Orlando, Valerio; Ovchinnikov, Dmitry A.; Pain, Arnab; Passier, Robert; Patrikakis, Margaret; Persson, Helena; Piazza, Silvano; Prendergast, James G D; Rackham, Owen J L; Ramilowski, Jordan A.; Rashid, Mamoon; Ravasi, Timothy; Rizzu, Patrizia; Roncador, Marco; Roy, Sugata; Rye, Morten B.; Saijyo, Eri; Sajantila, Antti; Saka, Akiko; Sakaguchi, Shimon; Sakai, Mizuho; Sato, Hiroki; Satoh, Hironori; Savvi, Suzana; Saxena, Alka; Schneider, Claudio; Schultes, Erik A.; Schulze-Tanzil, Gundula G.; Schwegmann, Anita; Sengstag, Thierry; Sheng, Guojun; Shimoji, Hisashi; Shimoni, Yishai; Shin, Jay W.; Simon, Christophe; Sugiyama, Daisuke; Sugiyama, Takaaki; Suzuki, Masanori; Suzuki, Naoko; Swoboda, Rolf K.; 't Hoen, Peter A C; Tagami, Michihira; Takahashi, Naoko; Takai, Jun; Tanaka, Hiroshi; Tatsukawa, Hideki; Tatum, Zuotian; Thompson, Mark; Toyoda, Hiroo; Toyoda, Tetsuro; Valen, Eivind; van de Wetering, Marc; van den Berg, Linda M.; Verardo, Roberto; Vijayan, Dipti; Vorontsov, Ilya E.; Wasserman, Wyeth W.; Watanabe, Shoko; Wells, Christine A.; Winteringham, Louise N.; Wolvetang, Ernst; Wood, Emily J.; Yamaguchi, Yoko; Yamamoto, Masayuki; Yoneda, Misako; Yonekura, Yohei; Yoshida, Shigehiro; Zabierowski, Suzan E.; Zhang, Peter G.; Zhao, Xiaobei; Zucchelli, Silvia; Summers, Kim M.; Suzuki, Harukazu; Daub, Carsten O.; Kawai, Jun; Heutink, Peter; Hide, Winston; Freeman, Tom C.; Lenhard, Boris; Bajic, Vladimir B.; Taylor, Martin S.; Makeev, Vsevolod J.; Sandelin, Albin Gustav; Hume, David A.; Carninci, Piero; Hayashizaki, Yoshihide.
In:
PLoS Biology, Vol. 13, No. 12, e1002315, 2015.
Research output: Contribution to journal › Journal article › Research › peer-review
Harvard
Hurst, LD, Ghanbarian, AT, Forrest, ARR, Huminiecki, L, Rehli, M, Kenneth Baillie, J, de Hoon, MJL, Haberle, V, Lassmann, T, Kulakovskiy, IV, Lizio, M, Itoh, M
, Andersson, R, Mungall, CJ, Meehan, TF, Schmeier, S, Bertin, N, Jørgensen, M, Dimont, E, Arner, E, Schmidl, C, Schaefer, U, Medvedeva, YA, Plessy, C, Vitezic, M, Severin, J, Semple, CA, Ishizu, Y, Young, RS, Francescatto, M, Alam, I, Albanese, D, Altschuler, GM, Arakawa, T, Archer, JAC, Arner, P, Babina, M, Baker, S, Balwierz, PJ, Beckhouse, AG, Pradhan, SB, Blake, JA, Blumenthal, A, Bodega, B, Bonetti, A, Briggs, J, Brombacher, F, Maxwell Burroughs, A, Califano, A, Cannistraci, CV, Carbajo, D, Chen, Y, Chierici, M, Ciani, Y, Clevers, HC, Dalla, E, Davis, CA, Detmar, M, Diehl, AD, Dohi, T, Drabløs, F, Edge, ASB, Edinger, M, Ekwall, K, Endoh, M, Enomoto, H, Fagiolini, M, Fairbairn, L, Fang, H, Farach-Carson, MC, Faulkner, GJ, Favorov, AV, Fisher, ME, Frith, MC, Fujita, R, Fukuda, S, Furlanello, C, Furuno, M, Furusawa, JI, Geijtenbeek, TB, Gibson, A, Gingeras, T, Goldowitz, D, Gough, J, Guhl, S, Guler, R, Gustincich, S, Ha, TJ, Hamaguchi, M, Hara, M, Harbers, M, Harshbarger, J, Hasegawa, A, Hasegawa, Y, Hashimoto, T, Herlyn, M, Hitchens, KJ, Ho Sui, SJ, Hofmann, OM, Hoof, I, Hori, F, Huminiecki, L, Iida, K, Ikawa, T, Jankovic, BR, Jia, H, Joshi, A, Jurman, G, Kaczkowski, B, Kai, C, Kaida, K, Kaiho, A, Kajiyama, K, Kanamori, MK, Kasianov, AS, Kasukawa, T, Katayama, S, Kato, S, Kawaguchi, S, Kawamoto, H, Kawamura, YI, Kawashima, T, Kempfle, JS, Kenna, TJ, Kere, J, Khachigian, LM, Kitamura, T, Peter Klinken, S, Knox, AJ, Kojima, M, Kojima, S, Kondo, N, Koseki, H, Koyasu, S, Krampitz, S, Kubosaki, A, Kwon, AT, Laros, JFJ, Lee, W, Lennartsson, A, Li, K, Lilje, B, Lipovich, L, Mackay, AS, Manabe, R, Mar, JC, Marchand, B, Mathelier, A, Mejhert, N, Meynert, A, Mizuno, Y, de Lima Morais, DA, Morikawa, H, Morimoto, M, Moro, K, Motakis, E, Motohashi, H, Mummery, CL, Murata, M, Nagao, SS, Nakachi, Y, Nakahara, F, Nakamura, T, Nakamura, Y, Nakazato, K, van Nimwegen, E, Ninomiya, N, Nishiyori, H, Noma, S, Nozaki, T, Ogishima, S, Ohkura, N, Ohmiya, H, Ohno, H, Ohshima, M, Okada, MH, Okazaki, Y, Orlando, V, Ovchinnikov, DA, Pain, A, Passier, R, Patrikakis, M, Persson, H, Piazza, S, Prendergast, JGD, Rackham, OJL, Ramilowski, JA, Rashid, M, Ravasi, T, Rizzu, P, Roncador, M, Roy, S, Rye, MB, Saijyo, E, Sajantila, A, Saka, A, Sakaguchi, S, Sakai, M, Sato, H, Satoh, H, Savvi, S, Saxena, A, Schneider, C, Schultes, EA, Schulze-Tanzil, GG, Schwegmann, A, Sengstag, T, Sheng, G, Shimoji, H, Shimoni, Y, Shin, JW, Simon, C, Sugiyama, D, Sugiyama, T, Suzuki, M, Suzuki, N, Swoboda, RK, 't Hoen, PAC, Tagami, M, Takahashi, N, Takai, J, Tanaka, H, Tatsukawa, H, Tatum, Z, Thompson, M, Toyoda, H, Toyoda, T, Valen, E, van de Wetering, M, van den Berg, LM, Verardo, R, Vijayan, D, Vorontsov, IE, Wasserman, WW, Watanabe, S, Wells, CA, Winteringham, LN, Wolvetang, E, Wood, EJ, Yamaguchi, Y, Yamamoto, M, Yoneda, M, Yonekura, Y, Yoshida, S, Zabierowski, SE, Zhang, PG, Zhao, X, Zucchelli, S, Summers, KM, Suzuki, H, Daub, CO, Kawai, J, Heutink, P, Hide, W, Freeman, TC, Lenhard, B, Bajic, VB, Taylor, MS, Makeev, VJ
, Sandelin, AG, Hume, DA, Carninci, P & Hayashizaki, Y 2015, '
The constrained maximal expression level owing to haploidy shapes gene content on the mammalian X chromosome',
PLoS Biology, vol. 13, no. 12, e1002315.
https://doi.org/10.1371/journal.pbio.1002315APA
Hurst, L. D., Ghanbarian, A. T., Forrest, A. R. R., Huminiecki, L., Rehli, M., Kenneth Baillie, J., de Hoon, M. J. L., Haberle, V., Lassmann, T., Kulakovskiy, I. V., Lizio, M., Itoh, M.
, Andersson, R., Mungall, C. J., Meehan, T. F., Schmeier, S., Bertin, N., Jørgensen, M., Dimont, E., ... Hayashizaki, Y. (2015).
The constrained maximal expression level owing to haploidy shapes gene content on the mammalian X chromosome.
PLoS Biology,
13(12), [e1002315].
https://doi.org/10.1371/journal.pbio.1002315Vancouver
Hurst LD, Ghanbarian AT, Forrest ARR, Huminiecki L, Rehli M, Kenneth Baillie J et al.
The constrained maximal expression level owing to haploidy shapes gene content on the mammalian X chromosome.
PLoS Biology. 2015;13(12). e1002315.
https://doi.org/10.1371/journal.pbio.1002315Author
Hurst, Laurence D. ; Ghanbarian, Avazeh T. ; Forrest, Alistair R R ; Huminiecki, Lukasz ; Rehli, Michael ; Kenneth Baillie, J. ; de Hoon, Michiel J L ; Haberle, Vanja ; Lassmann, Timo ; Kulakovskiy, Ivan V. ; Lizio, Marina ; Itoh, Masayoshi ; Andersson, Robin ; Mungall, Christopher J. ; Meehan, Terrence F. ; Schmeier, Sebastian ; Bertin, Nicolas ; Jørgensen, Mette ; Dimont, Emmanuel ; Arner, Erik ; Schmidl, Christian ; Schaefer, Ulf ; Medvedeva, Yulia A. ; Plessy, Charles ; Vitezic, Morana ; Severin, Jessica ; Semple, Colin A. ; Ishizu, Yuri ; Young, Robert S. ; Francescatto, Margherita ; Alam, Intikhab ; Albanese, Davide ; Altschuler, Gabriel M. ; Arakawa, Takahiro ; Archer, John A C ; Arner, Peter ; Babina, Magda ; Baker, Sarah ; Balwierz, Piotr J. ; Beckhouse, Anthony G. ; Pradhan, Swati Bhatt ; Blake, Judith A. ; Blumenthal, Antje ; Bodega, Beatrice ; Bonetti, Alessandro ; Briggs, James ; Brombacher, Frank ; Maxwell Burroughs, A. ; Califano, Andrea ; Cannistraci, Carlo V. ; Carbajo, Daniel ; Chen, Yun ; Chierici, Marco ; Ciani, Yari ; Clevers, Hans C. ; Dalla, Emiliano ; Davis, Carrie A. ; Detmar, Michael ; Diehl, Alexander D. ; Dohi, Taeko ; Drabløs, Finn ; Edge, Albert S B ; Edinger, Matthias ; Ekwall, Karl ; Endoh, Mitsuhiro ; Enomoto, Hideki ; Fagiolini, Michela ; Fairbairn, Lynsey ; Fang, Hai ; Farach-Carson, Mary C. ; Faulkner, Geoffrey J. ; Favorov, Alexander V. ; Fisher, Malcolm E. ; Frith, Martin C. ; Fujita, Rie ; Fukuda, Shiro ; Furlanello, Cesare ; Furuno, Masaaki ; Furusawa, Jun ichi ; Geijtenbeek, Teunis B. ; Gibson, Andrew ; Gingeras, Thomas ; Goldowitz, Daniel ; Gough, Julian ; Guhl, Sven ; Guler, Reto ; Gustincich, Stefano ; Ha, Thomas J. ; Hamaguchi, Masahide ; Hara, Mitsuko ; Harbers, Matthias ; Harshbarger, Jayson ; Hasegawa, Akira ; Hasegawa, Yuki ; Hashimoto, Takehiro ; Herlyn, Meenhard ; Hitchens, Kelly J. ; Ho Sui, Shannan J. ; Hofmann, Oliver M. ; Hoof, Ilka ; Hori, Fumi ; Huminiecki, Lukasz ; Iida, Kei ; Ikawa, Tomokatsu ; Jankovic, Boris R. ; Jia, Hui ; Joshi, Anagha ; Jurman, Giuseppe ; Kaczkowski, Bogumil ; Kai, Chieko ; Kaida, Kaoru ; Kaiho, Ai ; Kajiyama, Kazuhiro ; Kanamori, Mutsumi Katayama ; Kasianov, Artem S. ; Kasukawa, Takeya ; Katayama, Shintaro ; Kato, Sachi ; Kawaguchi, Shuji ; Kawamoto, Hiroshi ; Kawamura, Yuki I. ; Kawashima, Tsugumi ; Kempfle, Judith S. ; Kenna, Tony J. ; Kere, Juha ; Khachigian, Levon M. ; Kitamura, Toshio ; Peter Klinken, S. ; Knox, Alan J. ; Kojima, Miki ; Kojima, Soichi ; Kondo, Naoto ; Koseki, Haruhiko ; Koyasu, Shigeo ; Krampitz, Sarah ; Kubosaki, Atsutaka ; Kwon, Andrew T. ; Laros, Jeroen F J ; Lee, Weonju ; Lennartsson, Andreas ; Li, Kang ; Lilje, Berit ; Lipovich, Leonard ; Mackay, Alan sim ; Manabe, Riichiroh ; Mar, Jessica C. ; Marchand, Benoit ; Mathelier, Anthony ; Mejhert, Niklas ; Meynert, Alison ; Mizuno, Yosuke ; de Lima Morais, David A. ; Morikawa, Hiromasa ; Morimoto, Mitsuru ; Moro, Kazuyo ; Motakis, Efthymios ; Motohashi, Hozumi ; Mummery, Christine L. ; Murata, Mitsuyoshi ; Nagao, Sayaka Sato ; Nakachi, Yutaka ; Nakahara, Fumio ; Nakamura, Toshiyuki ; Nakamura, Yukio ; Nakazato, Kenichi ; van Nimwegen, Erik ; Ninomiya, Noriko ; Nishiyori, Hiromi ; Noma, Shohei ; Nozaki, Tadasuke ; Ogishima, Soichi ; Ohkura, Naganari ; Ohmiya, Hiroko ; Ohno, Hiroshi ; Ohshima, Mitsuhiro ; Okada, Mariko Hatakeyama ; Okazaki, Yasushi ; Orlando, Valerio ; Ovchinnikov, Dmitry A. ; Pain, Arnab ; Passier, Robert ; Patrikakis, Margaret ; Persson, Helena ; Piazza, Silvano ; Prendergast, James G D ; Rackham, Owen J L ; Ramilowski, Jordan A. ; Rashid, Mamoon ; Ravasi, Timothy ; Rizzu, Patrizia ; Roncador, Marco ; Roy, Sugata ; Rye, Morten B. ; Saijyo, Eri ; Sajantila, Antti ; Saka, Akiko ; Sakaguchi, Shimon ; Sakai, Mizuho ; Sato, Hiroki ; Satoh, Hironori ; Savvi, Suzana ; Saxena, Alka ; Schneider, Claudio ; Schultes, Erik A. ; Schulze-Tanzil, Gundula G. ; Schwegmann, Anita ; Sengstag, Thierry ; Sheng, Guojun ; Shimoji, Hisashi ; Shimoni, Yishai ; Shin, Jay W. ; Simon, Christophe ; Sugiyama, Daisuke ; Sugiyama, Takaaki ; Suzuki, Masanori ; Suzuki, Naoko ; Swoboda, Rolf K. ; 't Hoen, Peter A C ; Tagami, Michihira ; Takahashi, Naoko ; Takai, Jun ; Tanaka, Hiroshi ; Tatsukawa, Hideki ; Tatum, Zuotian ; Thompson, Mark ; Toyoda, Hiroo ; Toyoda, Tetsuro ; Valen, Eivind ; van de Wetering, Marc ; van den Berg, Linda M. ; Verardo, Roberto ; Vijayan, Dipti ; Vorontsov, Ilya E. ; Wasserman, Wyeth W. ; Watanabe, Shoko ; Wells, Christine A. ; Winteringham, Louise N. ; Wolvetang, Ernst ; Wood, Emily J. ; Yamaguchi, Yoko ; Yamamoto, Masayuki ; Yoneda, Misako ; Yonekura, Yohei ; Yoshida, Shigehiro ; Zabierowski, Suzan E. ; Zhang, Peter G. ; Zhao, Xiaobei ; Zucchelli, Silvia ; Summers, Kim M. ; Suzuki, Harukazu ; Daub, Carsten O. ; Kawai, Jun ; Heutink, Peter ; Hide, Winston ; Freeman, Tom C. ; Lenhard, Boris ; Bajic, Vladimir B. ; Taylor, Martin S. ; Makeev, Vsevolod J. ; Sandelin, Albin Gustav ; Hume, David A. ; Carninci, Piero ; Hayashizaki, Yoshihide. / The constrained maximal expression level owing to haploidy shapes gene content on the mammalian X chromosome. In: PLoS Biology. 2015 ; Vol. 13, No. 12.
Bibtex
@article{c03df45eefb646419c89b6b97b44bcec,
title = "The constrained maximal expression level owing to haploidy shapes gene content on the mammalian X chromosome",
abstract = "X chromosomes are unusual in many regards, not least of which is their nonrandom gene content. The causes of this bias are commonly discussed in the context of sexual antagonism and the avoidance of activity in the male germline. Here, we examine the notion that, at least in some taxa, functionally biased gene content may more profoundly be shaped by limits imposed on gene expression owing to haploid expression of the X chromosome. Notably, if the X, as in primates, is transcribed at rates comparable to the ancestral rate (per promoter) prior to the X chromosome formation, then the X is not a tolerable environment for genes with very high maximal net levels of expression, owing to transcriptional traffic jams. We test this hypothesis using The Encyclopedia of DNA Elements (ENCODE) and data from the Functional Annotation of the Mammalian Genome (FANTOM5) project. As predicted, the maximal expression of human X-linked genes is much lower than that of genes on autosomes: on average, maximal expression is three times lower on the X chromosome than on autosomes. Similarly, autosome-to-X retroposition events are associated with lower maximal expression of retrogenes on the X than seen for X-to-autosome retrogenes on autosomes. Also as expected, X-linked genes have a lesser degree of increase in gene expression than autosomal ones (compared to the human/Chimpanzee common ancestor) if highly expressed, but not if lowly expressed. The traffic jam model also explains the known lower breadth of expression for genes on the X (and the Z of birds), as genes with broad expression are, on average, those with high maximal expression. As then further predicted, highly expressed tissue-specific genes are also rare on the X and broadly expressed genes on the X tend to be lowly expressed, both indicating that the trend is shaped by the maximal expression level not the breadth of expression per se. Importantly, a limit to the maximal expression level explains biased tissue of expression profiles of X-linked genes. Tissues whose tissue-specific genes are very highly expressed (e.g., secretory tissues, tissues abundant in structural proteins) are also tissues in which gene expression is relatively rare on the X chromosome. These trends cannot be fully accounted for in terms of alternative models of biased expression. In conclusion, the notion that it is hard for genes on the Therian X to be highly expressed, owing to transcriptional traffic jams, provides a simple yet robustly supported rationale of many peculiar features of X{\textquoteright}s gene content, gene expression, and evolution.",
author = "Hurst, {Laurence D.} and Ghanbarian, {Avazeh T.} and Forrest, {Alistair R R} and Lukasz Huminiecki and Michael Rehli and {Kenneth Baillie}, J. and {de Hoon}, {Michiel J L} and Vanja Haberle and Timo Lassmann and Kulakovskiy, {Ivan V.} and Marina Lizio and Masayoshi Itoh and Robin Andersson and Mungall, {Christopher J.} and Meehan, {Terrence F.} and Sebastian Schmeier and Nicolas Bertin and Mette J{\o}rgensen and Emmanuel Dimont and Erik Arner and Christian Schmidl and Ulf Schaefer and Medvedeva, {Yulia A.} and Charles Plessy and Morana Vitezic and Jessica Severin and Semple, {Colin A.} and Yuri Ishizu and Young, {Robert S.} and Margherita Francescatto and Intikhab Alam and Davide Albanese and Altschuler, {Gabriel M.} and Takahiro Arakawa and Archer, {John A C} and Peter Arner and Magda Babina and Sarah Baker and Balwierz, {Piotr J.} and Beckhouse, {Anthony G.} and Pradhan, {Swati Bhatt} and Blake, {Judith A.} and Antje Blumenthal and Beatrice Bodega and Alessandro Bonetti and James Briggs and Frank Brombacher and {Maxwell Burroughs}, A. and Andrea Califano and Cannistraci, {Carlo V.} and Daniel Carbajo and Yun Chen and Marco Chierici and Yari Ciani and Clevers, {Hans C.} and Emiliano Dalla and Davis, {Carrie A.} and Michael Detmar and Diehl, {Alexander D.} and Taeko Dohi and Finn Drabl{\o}s and Edge, {Albert S B} and Matthias Edinger and Karl Ekwall and Mitsuhiro Endoh and Hideki Enomoto and Michela Fagiolini and Lynsey Fairbairn and Hai Fang and Farach-Carson, {Mary C.} and Faulkner, {Geoffrey J.} and Favorov, {Alexander V.} and Fisher, {Malcolm E.} and Frith, {Martin C.} and Rie Fujita and Shiro Fukuda and Cesare Furlanello and Masaaki Furuno and Furusawa, {Jun ichi} and Geijtenbeek, {Teunis B.} and Andrew Gibson and Thomas Gingeras and Daniel Goldowitz and Julian Gough and Sven Guhl and Reto Guler and Stefano Gustincich and Ha, {Thomas J.} and Masahide Hamaguchi and Mitsuko Hara and Matthias Harbers and Jayson Harshbarger and Akira Hasegawa and Yuki Hasegawa and Takehiro Hashimoto and Meenhard Herlyn and Hitchens, {Kelly J.} and {Ho Sui}, {Shannan J.} and Hofmann, {Oliver M.} and Ilka Hoof and Fumi Hori and Lukasz Huminiecki and Kei Iida and Tomokatsu Ikawa and Jankovic, {Boris R.} and Hui Jia and Anagha Joshi and Giuseppe Jurman and Bogumil Kaczkowski and Chieko Kai and Kaoru Kaida and Ai Kaiho and Kazuhiro Kajiyama and Kanamori, {Mutsumi Katayama} and Kasianov, {Artem S.} and Takeya Kasukawa and Shintaro Katayama and Sachi Kato and Shuji Kawaguchi and Hiroshi Kawamoto and Kawamura, {Yuki I.} and Tsugumi Kawashima and Kempfle, {Judith S.} and Kenna, {Tony J.} and Juha Kere and Khachigian, {Levon M.} and Toshio Kitamura and {Peter Klinken}, S. and Knox, {Alan J.} and Miki Kojima and Soichi Kojima and Naoto Kondo and Haruhiko Koseki and Shigeo Koyasu and Sarah Krampitz and Atsutaka Kubosaki and Kwon, {Andrew T.} and Laros, {Jeroen F J} and Weonju Lee and Andreas Lennartsson and Kang Li and Berit Lilje and Leonard Lipovich and Mackay, {Alan sim} and Riichiroh Manabe and Mar, {Jessica C.} and Benoit Marchand and Anthony Mathelier and Niklas Mejhert and Alison Meynert and Yosuke Mizuno and {de Lima Morais}, {David A.} and Hiromasa Morikawa and Mitsuru Morimoto and Kazuyo Moro and Efthymios Motakis and Hozumi Motohashi and Mummery, {Christine L.} and Mitsuyoshi Murata and Nagao, {Sayaka Sato} and Yutaka Nakachi and Fumio Nakahara and Toshiyuki Nakamura and Yukio Nakamura and Kenichi Nakazato and {van Nimwegen}, Erik and Noriko Ninomiya and Hiromi Nishiyori and Shohei Noma and Tadasuke Nozaki and Soichi Ogishima and Naganari Ohkura and Hiroko Ohmiya and Hiroshi Ohno and Mitsuhiro Ohshima and Okada, {Mariko Hatakeyama} and Yasushi Okazaki and Valerio Orlando and Ovchinnikov, {Dmitry A.} and Arnab Pain and Robert Passier and Margaret Patrikakis and Helena Persson and Silvano Piazza and Prendergast, {James G D} and Rackham, {Owen J L} and Ramilowski, {Jordan A.} and Mamoon Rashid and Timothy Ravasi and Patrizia Rizzu and Marco Roncador and Sugata Roy and Rye, {Morten B.} and Eri Saijyo and Antti Sajantila and Akiko Saka and Shimon Sakaguchi and Mizuho Sakai and Hiroki Sato and Hironori Satoh and Suzana Savvi and Alka Saxena and Claudio Schneider and Schultes, {Erik A.} and Schulze-Tanzil, {Gundula G.} and Anita Schwegmann and Thierry Sengstag and Guojun Sheng and Hisashi Shimoji and Yishai Shimoni and Shin, {Jay W.} and Christophe Simon and Daisuke Sugiyama and Takaaki Sugiyama and Masanori Suzuki and Naoko Suzuki and Swoboda, {Rolf K.} and {'t Hoen}, {Peter A C} and Michihira Tagami and Naoko Takahashi and Jun Takai and Hiroshi Tanaka and Hideki Tatsukawa and Zuotian Tatum and Mark Thompson and Hiroo Toyoda and Tetsuro Toyoda and Eivind Valen and {van de Wetering}, Marc and {van den Berg}, {Linda M.} and Roberto Verardo and Dipti Vijayan and Vorontsov, {Ilya E.} and Wasserman, {Wyeth W.} and Shoko Watanabe and Wells, {Christine A.} and Winteringham, {Louise N.} and Ernst Wolvetang and Wood, {Emily J.} and Yoko Yamaguchi and Masayuki Yamamoto and Misako Yoneda and Yohei Yonekura and Shigehiro Yoshida and Zabierowski, {Suzan E.} and Zhang, {Peter G.} and Xiaobei Zhao and Silvia Zucchelli and Summers, {Kim M.} and Harukazu Suzuki and Daub, {Carsten O.} and Jun Kawai and Peter Heutink and Winston Hide and Freeman, {Tom C.} and Boris Lenhard and Bajic, {Vladimir B.} and Taylor, {Martin S.} and Makeev, {Vsevolod J.} and Sandelin, {Albin Gustav} and Hume, {David A.} and Piero Carninci and Yoshihide Hayashizaki",
year = "2015",
doi = "10.1371/journal.pbio.1002315",
language = "English",
volume = "13",
journal = "PLoS Biology",
issn = "1544-9173",
publisher = "Public Library of Science",
number = "12",
}
RIS
TY - JOUR
T1 - The constrained maximal expression level owing to haploidy shapes gene content on the mammalian X chromosome
AU - Hurst, Laurence D.
AU - Ghanbarian, Avazeh T.
AU - Forrest, Alistair R R
AU - Huminiecki, Lukasz
AU - Rehli, Michael
AU - Kenneth Baillie, J.
AU - de Hoon, Michiel J L
AU - Haberle, Vanja
AU - Lassmann, Timo
AU - Kulakovskiy, Ivan V.
AU - Lizio, Marina
AU - Itoh, Masayoshi
AU - Andersson, Robin
AU - Mungall, Christopher J.
AU - Meehan, Terrence F.
AU - Schmeier, Sebastian
AU - Bertin, Nicolas
AU - Jørgensen, Mette
AU - Dimont, Emmanuel
AU - Arner, Erik
AU - Schmidl, Christian
AU - Schaefer, Ulf
AU - Medvedeva, Yulia A.
AU - Plessy, Charles
AU - Vitezic, Morana
AU - Severin, Jessica
AU - Semple, Colin A.
AU - Ishizu, Yuri
AU - Young, Robert S.
AU - Francescatto, Margherita
AU - Alam, Intikhab
AU - Albanese, Davide
AU - Altschuler, Gabriel M.
AU - Arakawa, Takahiro
AU - Archer, John A C
AU - Arner, Peter
AU - Babina, Magda
AU - Baker, Sarah
AU - Balwierz, Piotr J.
AU - Beckhouse, Anthony G.
AU - Pradhan, Swati Bhatt
AU - Blake, Judith A.
AU - Blumenthal, Antje
AU - Bodega, Beatrice
AU - Bonetti, Alessandro
AU - Briggs, James
AU - Brombacher, Frank
AU - Maxwell Burroughs, A.
AU - Califano, Andrea
AU - Cannistraci, Carlo V.
AU - Carbajo, Daniel
AU - Chen, Yun
AU - Chierici, Marco
AU - Ciani, Yari
AU - Clevers, Hans C.
AU - Dalla, Emiliano
AU - Davis, Carrie A.
AU - Detmar, Michael
AU - Diehl, Alexander D.
AU - Dohi, Taeko
AU - Drabløs, Finn
AU - Edge, Albert S B
AU - Edinger, Matthias
AU - Ekwall, Karl
AU - Endoh, Mitsuhiro
AU - Enomoto, Hideki
AU - Fagiolini, Michela
AU - Fairbairn, Lynsey
AU - Fang, Hai
AU - Farach-Carson, Mary C.
AU - Faulkner, Geoffrey J.
AU - Favorov, Alexander V.
AU - Fisher, Malcolm E.
AU - Frith, Martin C.
AU - Fujita, Rie
AU - Fukuda, Shiro
AU - Furlanello, Cesare
AU - Furuno, Masaaki
AU - Furusawa, Jun ichi
AU - Geijtenbeek, Teunis B.
AU - Gibson, Andrew
AU - Gingeras, Thomas
AU - Goldowitz, Daniel
AU - Gough, Julian
AU - Guhl, Sven
AU - Guler, Reto
AU - Gustincich, Stefano
AU - Ha, Thomas J.
AU - Hamaguchi, Masahide
AU - Hara, Mitsuko
AU - Harbers, Matthias
AU - Harshbarger, Jayson
AU - Hasegawa, Akira
AU - Hasegawa, Yuki
AU - Hashimoto, Takehiro
AU - Herlyn, Meenhard
AU - Hitchens, Kelly J.
AU - Ho Sui, Shannan J.
AU - Hofmann, Oliver M.
AU - Hoof, Ilka
AU - Hori, Fumi
AU - Huminiecki, Lukasz
AU - Iida, Kei
AU - Ikawa, Tomokatsu
AU - Jankovic, Boris R.
AU - Jia, Hui
AU - Joshi, Anagha
AU - Jurman, Giuseppe
AU - Kaczkowski, Bogumil
AU - Kai, Chieko
AU - Kaida, Kaoru
AU - Kaiho, Ai
AU - Kajiyama, Kazuhiro
AU - Kanamori, Mutsumi Katayama
AU - Kasianov, Artem S.
AU - Kasukawa, Takeya
AU - Katayama, Shintaro
AU - Kato, Sachi
AU - Kawaguchi, Shuji
AU - Kawamoto, Hiroshi
AU - Kawamura, Yuki I.
AU - Kawashima, Tsugumi
AU - Kempfle, Judith S.
AU - Kenna, Tony J.
AU - Kere, Juha
AU - Khachigian, Levon M.
AU - Kitamura, Toshio
AU - Peter Klinken, S.
AU - Knox, Alan J.
AU - Kojima, Miki
AU - Kojima, Soichi
AU - Kondo, Naoto
AU - Koseki, Haruhiko
AU - Koyasu, Shigeo
AU - Krampitz, Sarah
AU - Kubosaki, Atsutaka
AU - Kwon, Andrew T.
AU - Laros, Jeroen F J
AU - Lee, Weonju
AU - Lennartsson, Andreas
AU - Li, Kang
AU - Lilje, Berit
AU - Lipovich, Leonard
AU - Mackay, Alan sim
AU - Manabe, Riichiroh
AU - Mar, Jessica C.
AU - Marchand, Benoit
AU - Mathelier, Anthony
AU - Mejhert, Niklas
AU - Meynert, Alison
AU - Mizuno, Yosuke
AU - de Lima Morais, David A.
AU - Morikawa, Hiromasa
AU - Morimoto, Mitsuru
AU - Moro, Kazuyo
AU - Motakis, Efthymios
AU - Motohashi, Hozumi
AU - Mummery, Christine L.
AU - Murata, Mitsuyoshi
AU - Nagao, Sayaka Sato
AU - Nakachi, Yutaka
AU - Nakahara, Fumio
AU - Nakamura, Toshiyuki
AU - Nakamura, Yukio
AU - Nakazato, Kenichi
AU - van Nimwegen, Erik
AU - Ninomiya, Noriko
AU - Nishiyori, Hiromi
AU - Noma, Shohei
AU - Nozaki, Tadasuke
AU - Ogishima, Soichi
AU - Ohkura, Naganari
AU - Ohmiya, Hiroko
AU - Ohno, Hiroshi
AU - Ohshima, Mitsuhiro
AU - Okada, Mariko Hatakeyama
AU - Okazaki, Yasushi
AU - Orlando, Valerio
AU - Ovchinnikov, Dmitry A.
AU - Pain, Arnab
AU - Passier, Robert
AU - Patrikakis, Margaret
AU - Persson, Helena
AU - Piazza, Silvano
AU - Prendergast, James G D
AU - Rackham, Owen J L
AU - Ramilowski, Jordan A.
AU - Rashid, Mamoon
AU - Ravasi, Timothy
AU - Rizzu, Patrizia
AU - Roncador, Marco
AU - Roy, Sugata
AU - Rye, Morten B.
AU - Saijyo, Eri
AU - Sajantila, Antti
AU - Saka, Akiko
AU - Sakaguchi, Shimon
AU - Sakai, Mizuho
AU - Sato, Hiroki
AU - Satoh, Hironori
AU - Savvi, Suzana
AU - Saxena, Alka
AU - Schneider, Claudio
AU - Schultes, Erik A.
AU - Schulze-Tanzil, Gundula G.
AU - Schwegmann, Anita
AU - Sengstag, Thierry
AU - Sheng, Guojun
AU - Shimoji, Hisashi
AU - Shimoni, Yishai
AU - Shin, Jay W.
AU - Simon, Christophe
AU - Sugiyama, Daisuke
AU - Sugiyama, Takaaki
AU - Suzuki, Masanori
AU - Suzuki, Naoko
AU - Swoboda, Rolf K.
AU - 't Hoen, Peter A C
AU - Tagami, Michihira
AU - Takahashi, Naoko
AU - Takai, Jun
AU - Tanaka, Hiroshi
AU - Tatsukawa, Hideki
AU - Tatum, Zuotian
AU - Thompson, Mark
AU - Toyoda, Hiroo
AU - Toyoda, Tetsuro
AU - Valen, Eivind
AU - van de Wetering, Marc
AU - van den Berg, Linda M.
AU - Verardo, Roberto
AU - Vijayan, Dipti
AU - Vorontsov, Ilya E.
AU - Wasserman, Wyeth W.
AU - Watanabe, Shoko
AU - Wells, Christine A.
AU - Winteringham, Louise N.
AU - Wolvetang, Ernst
AU - Wood, Emily J.
AU - Yamaguchi, Yoko
AU - Yamamoto, Masayuki
AU - Yoneda, Misako
AU - Yonekura, Yohei
AU - Yoshida, Shigehiro
AU - Zabierowski, Suzan E.
AU - Zhang, Peter G.
AU - Zhao, Xiaobei
AU - Zucchelli, Silvia
AU - Summers, Kim M.
AU - Suzuki, Harukazu
AU - Daub, Carsten O.
AU - Kawai, Jun
AU - Heutink, Peter
AU - Hide, Winston
AU - Freeman, Tom C.
AU - Lenhard, Boris
AU - Bajic, Vladimir B.
AU - Taylor, Martin S.
AU - Makeev, Vsevolod J.
AU - Sandelin, Albin Gustav
AU - Hume, David A.
AU - Carninci, Piero
AU - Hayashizaki, Yoshihide
PY - 2015
Y1 - 2015
N2 - X chromosomes are unusual in many regards, not least of which is their nonrandom gene content. The causes of this bias are commonly discussed in the context of sexual antagonism and the avoidance of activity in the male germline. Here, we examine the notion that, at least in some taxa, functionally biased gene content may more profoundly be shaped by limits imposed on gene expression owing to haploid expression of the X chromosome. Notably, if the X, as in primates, is transcribed at rates comparable to the ancestral rate (per promoter) prior to the X chromosome formation, then the X is not a tolerable environment for genes with very high maximal net levels of expression, owing to transcriptional traffic jams. We test this hypothesis using The Encyclopedia of DNA Elements (ENCODE) and data from the Functional Annotation of the Mammalian Genome (FANTOM5) project. As predicted, the maximal expression of human X-linked genes is much lower than that of genes on autosomes: on average, maximal expression is three times lower on the X chromosome than on autosomes. Similarly, autosome-to-X retroposition events are associated with lower maximal expression of retrogenes on the X than seen for X-to-autosome retrogenes on autosomes. Also as expected, X-linked genes have a lesser degree of increase in gene expression than autosomal ones (compared to the human/Chimpanzee common ancestor) if highly expressed, but not if lowly expressed. The traffic jam model also explains the known lower breadth of expression for genes on the X (and the Z of birds), as genes with broad expression are, on average, those with high maximal expression. As then further predicted, highly expressed tissue-specific genes are also rare on the X and broadly expressed genes on the X tend to be lowly expressed, both indicating that the trend is shaped by the maximal expression level not the breadth of expression per se. Importantly, a limit to the maximal expression level explains biased tissue of expression profiles of X-linked genes. Tissues whose tissue-specific genes are very highly expressed (e.g., secretory tissues, tissues abundant in structural proteins) are also tissues in which gene expression is relatively rare on the X chromosome. These trends cannot be fully accounted for in terms of alternative models of biased expression. In conclusion, the notion that it is hard for genes on the Therian X to be highly expressed, owing to transcriptional traffic jams, provides a simple yet robustly supported rationale of many peculiar features of X’s gene content, gene expression, and evolution.
AB - X chromosomes are unusual in many regards, not least of which is their nonrandom gene content. The causes of this bias are commonly discussed in the context of sexual antagonism and the avoidance of activity in the male germline. Here, we examine the notion that, at least in some taxa, functionally biased gene content may more profoundly be shaped by limits imposed on gene expression owing to haploid expression of the X chromosome. Notably, if the X, as in primates, is transcribed at rates comparable to the ancestral rate (per promoter) prior to the X chromosome formation, then the X is not a tolerable environment for genes with very high maximal net levels of expression, owing to transcriptional traffic jams. We test this hypothesis using The Encyclopedia of DNA Elements (ENCODE) and data from the Functional Annotation of the Mammalian Genome (FANTOM5) project. As predicted, the maximal expression of human X-linked genes is much lower than that of genes on autosomes: on average, maximal expression is three times lower on the X chromosome than on autosomes. Similarly, autosome-to-X retroposition events are associated with lower maximal expression of retrogenes on the X than seen for X-to-autosome retrogenes on autosomes. Also as expected, X-linked genes have a lesser degree of increase in gene expression than autosomal ones (compared to the human/Chimpanzee common ancestor) if highly expressed, but not if lowly expressed. The traffic jam model also explains the known lower breadth of expression for genes on the X (and the Z of birds), as genes with broad expression are, on average, those with high maximal expression. As then further predicted, highly expressed tissue-specific genes are also rare on the X and broadly expressed genes on the X tend to be lowly expressed, both indicating that the trend is shaped by the maximal expression level not the breadth of expression per se. Importantly, a limit to the maximal expression level explains biased tissue of expression profiles of X-linked genes. Tissues whose tissue-specific genes are very highly expressed (e.g., secretory tissues, tissues abundant in structural proteins) are also tissues in which gene expression is relatively rare on the X chromosome. These trends cannot be fully accounted for in terms of alternative models of biased expression. In conclusion, the notion that it is hard for genes on the Therian X to be highly expressed, owing to transcriptional traffic jams, provides a simple yet robustly supported rationale of many peculiar features of X’s gene content, gene expression, and evolution.
U2 - 10.1371/journal.pbio.1002315
DO - 10.1371/journal.pbio.1002315
M3 - Journal article
C2 - 26685068
AN - SCOPUS:84969295765
VL - 13
JO - PLoS Biology
JF - PLoS Biology
SN - 1544-9173
IS - 12
M1 - e1002315
ER -
