September 9, 2014 u vol. 111 u no. 36 u 12955–13242

Cover image: Pictured is an inhibitory interneuron from the dentate gyrus, a region of the hippocampus containing neuronal assemblies that encode memories to locations in the en- vironment. Thomas Hainmüller et al. examined synaptic connections between neuronal assemblies and interneurons of the dentate gyrus in vitro to investigate the molecular mech- anisms that underlie synaptic plasticity in the interneurons. The strength of synaptic con- nections between the assemblies and the interneurons depended on activation of calcium ion- permeable glutamate receptors in the interneuron that activate protein kinase C to induce synaptic plasticity. See the article by Hainmüller et al. on pages 13211–13216. Image courtesy of Thomas Hainmüller. From the Cover

13211 Mechanism of memory formation 12974 Synchronizing musical rhythms 13122 Primitive fractal animal body plans 13187 Bacterial defense against neutrophils 13223 Hunting and bighorn sheep body mass

Contents COMMENTARIES

12960 Interplay of synchronized music Chung-Kang Peng THIS WEEK IN PNAS See companion article on page 12974

12962 Modeling morphological diversity in the oldest large 12955 In This Issue multicellular organisms Marc Laflamme See companion article on page 13122 LETTER (ONLINE ONLY) 12964 Managing wildlife for ecological, socioeconomic, and evolutionary sustainability E3755 Intraoperative cell-cycle analysis to guide brain Nils Bunnefeld and Aidan Keane tumor removal See companion article on page 13223 George Vartholomatos, George Alexiou, Anna Batistatou, and Athanasios P. Kyritsis

PNAS PLUS INNER WORKINGS—An over-the-shoulder look at scientists at work

12966 Significance Statements 12957 Inner Workings: The strictest biosafety Brief statements written by the authors about the significance of Amber Dance their papers.

QNAS PHYSICAL SCIENCES 12958 QnAs with Fred Gage Prashant Nair APPLIED MATHEMATICS 12968 Potentially singular solutions of the 3D axisymmetric Euler equations Free online through the PNAS open access option. Guo Luo and Thomas Y. Hou

PNAS u September 9, 2014 u vol. 111 u no. 36 u iii–vii Downloaded by guest on September 24, 2021 APPLIED PHYSICAL SCIENCES SOCIAL SCIENCES 12974 Synchronization in human musical rhythms and mutually interacting complex systems Holger Hennig ANTHROPOLOGY See Commentary on page 12960 12986 Age of Barrier Canyon-style rock art constrained by cross-cutting relations and luminescence 12980 Noncontact orientation of objects in three-dimensional dating techniques space using magnetic levitation Joel L. Pederson, Melissa S. Chapot, Steven R. Simms, Anand Bala Subramaniam, Dian Yang, Hai-Dong Yu, Reza Sohbati, Tammy M. Rittenour, Andrew S. Murray, Alex Nemiroski, Simon Tricard, Audrey K. Ellerbee, and Gary Cox Siowling Soh, and George M. Whitesides 13010 Metabolic costs and evolutionary implications of human brain development Christopher W. Kuzawa, Harry T. Chugani, Lawrence I. E3825 Design of donecopride, a dual serotonin subtype Grossman, Leonard Lipovich, Otto Muzik, Patrick R. Hof, 4 receptor agonist/acetylcholinesterase inhibitor Derek E. Wildman, Chet C. Sherwood, William R. Leonard, with potential interest for Alzheimer’s and Nicholas Lange disease treatment Cédric Lecoutey, Damien Hedou, Thomas Freret, Patrizia SUSTAINABILITY SCIENCE Giannoni, Florence Gaven, Marc Since, Valentine 13016 Linking knowledge and action through mental models Bouet, Céline Ballandonne, Sophie Corvaisier, Aurélie of sustainable agriculture Malzert Fréon, Serge Mignani, Thierry Cresteil, Matthew Hoffman, Mark Lubell, and Vicken Hillis Michel Boulouard, Sylvie Claeysen, Christophe Rochais, and Patrick Dallemagne 13117 Illegal killing for ivory drives global decline in African elephants 13235 Surprisal analysis characterizes the free energy George Wittemyer, Joseph M. Northrup, Julian Blanc, time course of cancer cells undergoing Iain Douglas-Hamilton, Patrick Omondi, epithelial-to-mesenchymal transition and Kenneth P. Burnham Sohila Zadran, Rameshkumar Arumugam, Harvey Herschman, Michael E. Phelps, and R. D. Levine BIOLOGICAL SCIENCES

EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES ANTHROPOLOGY 12986 Age of Barrier Canyon-style rock art constrained by cross-cutting relations and luminescence 13022 New high-resolution computed tomography data of the dating techniques Taung partial cranium and endocast and their bearing Joel L. Pederson, Melissa S. Chapot, Steven R. Simms, on metopism and hominin brain evolution Reza Sohbati, Tammy M. Rittenour, Andrew S. Murray, Ralph L. Holloway, Douglas C. Broadfield, and Gary Cox and Kristian J. Carlson

BIOCHEMISTRY ENGINEERING E3756 The class III from Neisseria 12992 Cell separation using tilted-angle standing surface bacilliformis can utilize thioredoxin as a reductant acoustic waves Yifeng Wei, Michael A. Funk, Leonardo A. Rosado, Xiaoyun Ding, Zhangli Peng, Sz-Chin Steven Lin, Jiyeon Baek, Catherine L. Drennan, Michela Geri, Sixing Li, Peng Li, Yuchao and JoAnne Stubbe Chen, Ming Dao, Subra Suresh, and Tony Jun Huang 13028 Structural basis for the fast self-cleavage reaction catalyzed by the twister ribozyme 12998 Adaptive optoelectronic camouflage systems with Daniel Eiler, Jimin Wang, and Thomas A. Steitz designs inspired by cephalopod skins Cunjiang Yu, Yuhang Li, Xun Zhang, Xian 13034 Directed evolution of a far-red fluorescent rhodopsin Huang, Viktor Malyarchuk, Shuodao Wang, R. Scott McIsaac, Martin K. M. Engqvist, Timothy Wannier, Yan Shi, Li Gao, Yewang Su, Yihui Zhang, Adam Z. Rosenthal, Lukas Herwig, Nicholas C. Flytzanis, Hangxun Xu, Roger T. Hanlon, Yonggang Eleonora S. Imasheva, Janos K. Lanyi, Sergei P. Balashov, Huang, and John A. Rogers Viviana Gradinaru, and Frances H. Arnold 13040 Ligand- and mutation-induced conformational selection PHYSICS in the CCR5 chemokine G protein-coupled receptor Ravinder Abrol, Bartosz Trzaskowski, William A. Goddard III, 13004 Nonlinear conduction via solitons in a topological Alexandre Nesterov, Ivan Olave, and Christopher Irons mechanical insulator Bryan Gin-ge Chen, Nitin Upadhyaya, 13046 Unfolded protein response activation reduces secretion and Vincenzo Vitelli and extracellular aggregation of amyloidogenic immunoglobulin light chain 13111 The transition between the niche and neutral regimes Christina B. Cooley, Lisa M. Ryno, Lars Plate, in ecology Gareth J. Morgan, John D. Hulleman, Jeffery W. Kelly, Charles K. Fisher and Pankaj Mehta and R. Luke Wiseman

iv u www.pnas.org Downloaded by guest on September 24, 2021 BIOPHYSICS AND COMPUTATIONAL BIOLOGY 13093 Optimized two-color super resolution imaging of Drp1 13052 Dynamic hydration shell restores Kauzmann’s 1959 during mitochondrial fission with a slow-switching explanation of how the hydrophobic factor drives Dronpa variant protein folding Alyssa B. Rosenbloom, Sang-Hyuk Lee, Milton To, Robert L. Baldwin Antony Lee, Jae Yen Shin, and Carlos Bustamante 13057 Local anesthetic and antiepileptic drug access and binding to a bacterial voltage-gated sodium channel DEVELOPMENTAL BIOLOGY Céline Boiteux, Igor Vorobyov, Robert J. French, 13099 Custos controls β-catenin to regulate head development Christopher French, Vladimir Yarov-Yarovoy, during vertebrate embryogenesis and Toby W. Allen Yuko Komiya, Noopur Mandrekar, Akira Sato, Igor B. Dawid, 13063 Nanoscale structure of the BMP antagonist chordin and Raymond Habas supports cooperative BMP binding 13105 Transmission of a signal that synchronizes Helen Troilo, Alexandra V. Zuk, Richard B. cell movements in swarms of Tunnicliffe, Alexander P. Wohl, Richard Berry, Myxococcus xanthus Richard F. Collins, Thomas A. Jowitt, Gerhard Sengle, Dale Kaiser and Hans Warrick and Clair Baldock 13069 Direct single-molecule observation of calcium-dependent misfolding in human neuronal ECOLOGY calcium sensor-1 13111 The transition between the niche and neutral regimes Pétur O. Heidarsson, Mohsin M. Naqvi, Mariela R. in ecology Otazo, Alessandro Mossa, Birthe B. Kragelund, Charles K. Fisher and Pankaj Mehta and Ciro Cecconi 13117 Illegal killing for ivory drives global decline in 13075 Three-dimensional cell body shape dictates the African elephants onset of traction force generation and growth of George Wittemyer, Joseph M. Northrup, Julian Blanc, focal adhesions Iain Douglas-Hamilton, Patrick Omondi, Jonathan Fouchard, Célian Bimbard, Nathalie Bufi, Pauline and Kenneth P. Burnham Durand-Smet, Amsha Proag, Alain Richert, Olivier Cardoso, and Atef Asnacios EVOLUTION

CELL BIOLOGY 13122 Fractal branching organizations of Ediacaran rangeomorph fronds reveal a lost Proterozoic – E3766 The Cap1 claudin-4 regulatory pathway is important for body plan renal chloride reabsorption and blood Jennifer F. Hoyal Cuthill and Simon Conway Morris pressure regulation See Commentary on page 12962 Yongfeng Gong, Miao Yu, Jing Yang, Ernie Gonzales, Ronaldo Perez, Mingli Hou, Piyush Tripathi, Kathleen S. Hering-Smith, L. Lee Hamm, and Jianghui Hou GENETICS E3775 Transcription factor PREP1 induces EMT and metastasis 13127 Rare variants in PPARG with decreased activity in by controlling the TGF-β–SMAD3 pathway in non-small adipocyte differentiation are associated with cell lung adenocarcinoma increased risk of type 2 diabetes Maurizio Risolino, Nadia Mandia, Francescopaolo Iavarone, Amit R. Majithia, Jason Flannick, Peter Shahinian, Leila Dardaei, Elena Longobardi, Serena Fernandez, Michael Guo, Mark-Anthony Bray, Pierre Fontanillas, Francesco Talotta, Fabrizio Bianchi, Federica Pisati, Lorenzo Stacey B. Gabriel, GoT2D Consortium, NHGRI Spaggiari, Patrick N. Harter, Michel Mittelbronn, Dorothea JHS/FHS Allelic Spectrum Project, SIGMA T2D Schulte, Mariarosaria Incoronato, Pier Paolo Di Fiore, Consortium, T2D-GENES Consortium, Evan D. Rosen, Francesco Blasi, and Pasquale Verde and David Altshuler 12992 Cell separation using tilted-angle standing surface acoustic waves IMMUNOLOGY AND INFLAMMATION Xiaoyun Ding, Zhangli Peng, Sz-Chin Steven Lin, Michela Geri, Sixing Li, Peng Li, Yuchao 13133 Induction of broadly cross-reactive antibody responses Chen, Ming Dao, Subra Suresh, to the influenza HA stem region following H5N1 and Tony Jun Huang vaccination in humans Ali H. Ellebedy, Florian Krammer, Gui-Mei Li, 13081 Nonlytic viral spread enhanced by autophagy Matthew S. Miller, Christopher Chiu, Jens Wrammert, components Cathy Y. Chang, Carl W. Davis, Megan McCausland, Sara Whitney Bird, Nathaniel D. Maynard, Markus W. Covert, Rivka Elbein, Srilatha Edupuganti, Paul Spearman, and Karla Kirkegaard Sarah F. Andrews, Patrick C. Wilson, Adolfo García-Sastre, Mark J. Mulligan, Aneesh K. Mehta, Peter Palese, 13087 The Two-pore channel (TPC) interactome unmasks and Rafi Ahmed isoform-specific roles for TPCs in endolysosomal morphology and cell pigmentation 13139 Diversity and clonal selection in the human Yaping Lin-Moshier, Michael V. Keebler, Robert Hooper, T-cell repertoire Michael J. Boulware, Xiaolong Liu, Dev Churamani, Qian Qi, Yi Liu, Yong Cheng, Jacob Glanville, David Zhang, Mary E. Abood, Timothy F. Walseth, Eugen Brailoiu, Ji-Yeun Lee, Richard A. Olshen, Cornelia M. Weyand, Sandip Patel, and Jonathan S. Marchant Scott D. Boyd, and Jörg J. Goronzy

PNAS u September 9, 2014 u vol. 111 u no. 36 u v Downloaded by guest on September 24, 2021 13145 Commensal bacteria protect against food NEUROSCIENCE allergen sensitization E3805 Ultrafast tissue staining with chemical tags Andrew T. Stefka, Taylor Feehley, Prabhanshu Tripathi, Johannes Kohl, Julian Ng, Sebastian Cachero, Ju Qiu, Kathy McCoy, Sarkis K. Mazmanian, Melissa Y. Ernesto Ciabatti, Michael-John Dolan, Ben Tjota, Goo-Young Seo, Severine Cao, Betty R. Theriault, Sutcliffe, Adam Tozer, Sabine Ruehle, Daniel Krueger, Dionysios A. Antonopoulos, Liang Zhou, Eugene B. Chang, Shahar Frechter, Tiago Branco, Marco Tripodi, Yang-Xin Fu, and Cathryn R. Nagler and Gregory S. X. E. Jefferis

E3815 Temporally defined neocortical translation and MEDICAL SCIENCES polysome assembly are determined by the RNA-binding E3785 Src promotes GTPase activity of Ras via tyrosine protein Hu antigen R 32 phosphorylation Matthew L. Kraushar, Kevin Thompson, H. R. Sagara Severa Bunda, Pardeep Heir, Tharan Srikumar, Jonathan D. Wijeratne, Barbara Viljetic, Kristina Sakers, Justin W. Cook, Kelly Burrell, Yoshihito Kano, Jeffrey E. Lee, Gelareh Marson, Dimitris L. Kontoyiannis, Steven Buyske, Zadeh, Brian Raught, and Michael Ohh Ronald P. Hart, and Mladen-Roko Rasin 13151 Broadly neutralizing antibodies suppress HIV in the 13010 Metabolic costs and evolutionary implications of human persistent viral reservoir brain development Tae-Wook Chun, Danielle Murray, Jesse S. Justement, Jana Christopher W. Kuzawa, Harry T. Chugani, Lawrence I. Blazkova, Claire W. Hallahan, Olivia Fankuchen, Kathleen Grossman, Leonard Lipovich, Otto Muzik, Patrick R. Hof, Gittens, Erika Benko, Colin Kovacs, Susan Moir, Derek E. Wildman, Chet C. Sherwood, William R. Leonard, and Anthony S. Fauci and Nicholas Lange 13157 RNA-guided endonuclease provides a 13193 MC4R-expressing glutamatergic neurons in the therapeutic strategy to cure latent paraventricular hypothalamus regulate feeding herpesviridae infection and are synaptically connected to the Jianbin Wang and Stephen R. Quake parabrachial nucleus Bhavik P. Shah, Linh Vong, David P. Olson, Shuichi 13163 Ghrelin promotes hepatic lipogenesis by activation of Koda, Michael J. Krashes, Chianping Ye, Zongfang Yang, γ mTOR-PPAR signaling pathway Patrick M. Fuller, Joel K. Elmquist, Ziru Li, Geyang Xu, Yan Qin, Chao Zhang, Hong Tang, and Bradford B. Lowell Yue Yin, Xinxin Xiang, Yin Li, Jing Zhao, Michael Mulholland, and Weizhen Zhang 13199 Overactivation of corticotropin-releasing factor receptor type 1 and aquaporin-4 by hypoxia induces cerebral edema MICROBIOLOGY Shao-Jun Chen, Jia-Fang Yang, Fan-Ping Kong, Ji-Long Ren, Ke Hao, Min Li, Yuan Yuan, Xin-Can Chen, E3795 Efficient replication of a paramyxovirus independent of full zippering of the fusion protein six-helix Ri-Sheng Yu, Jun-Fa Li, Gareth Leng, Xue-Qun Chen, bundle domain and Ji-Zeng Du Melinda A. Brindley, Philippe Plattet, 13205 Ubiquitin E3 ligase Nedd4-1 acts as a downstream target and Richard Karl Plemper of PI3K/PTEN-mTORC1 signaling to promote 13169 Attenuation of human respiratory syncytial virus by neurite growth genome-scale codon-pair deoptimization Hung-En Hsia, Rohit Kumar, Rossella Luca, Cyril Le Nouën, Linda G. Brock, Cindy Luongo, Thomas Michiko Takeda, Julien Courchet, Jonathan McCarty, Lijuan Yang, Masfique Mehedi, Eckard Wimmer, Nakashima, Shumin Wu, Sandra Goebbels, Steffen Mueller, Peter L. Collins, Ursula J. Buchholz, Wenlin An, Britta J. Eickholt, Franck Polleux, and Joshua M. DiNapoli Daniela Rotin, Hong Wu, Moritz J. Rossner, Claudia Bagni, Jeong-Seop Rhee, Nils Brose, 13175 Inhibition of Borna disease virus replication by an and Hiroshi Kawabe endogenous bornavirus-like element in the ground squirrel genome 13211 Joint CP-AMPA and group I mGlu receptor activation is Kan Fujino, Masayuki Horie, Tomoyuki Honda, required for synaptic plasticity in dentate gyrus Dana K. Merriman, and Keizo Tomonaga fast-spiking interneurons Thomas Hainmüller, Kerstin Krieglstein, Akos Kulik, 13181 Enterotoxicity of a nonribosomal peptide causes and Marlene Bartos antibiotic-associated colitis Georg Schneditz, Jana Rentner, Sandro Roier, Jakob Pletz, Kathrin A. T. Herzog, Roland Bücker, Hanno Troeger, Stefan Schild, Hansjörg Weber, Rolf Breinbauer, E3825 Design of donecopride, a dual serotonin subtype Gregor Gorkiewicz, Christoph Högenauer, 4 receptor agonist/acetylcholinesterase inhibitor and Ellen L. Zechner with potential interest for Alzheimer’s 13187 Staphylococcus aureus secretes a unique class of disease treatment neutrophil serine protease inhibitors Cédric Lecoutey, Damien Hedou, Thomas Freret, Patrizia Daphne A. C. Stapels, Kasra X. Ramyar, Markus Bischoff, Giannoni, Florence Gaven, Marc Since, Valentine Maren von Köckritz-Blickwede, Fin J. Milder, Maartje Bouet, Céline Ballandonne, Sophie Corvaisier, Aurélie Ruyken, Janina Eisenbeis, William J. McWhorter, Mathias Malzert Fréon, Serge Mignani, Thierry Cresteil, Herrmann, Kok P. M. van Kessel, Brian V. Geisbrecht, Michel Boulouard, Sylvie Claeysen, Christophe and Suzan H. M. Rooijakkers Rochais, and Patrick Dallemagne

vi u www.pnas.org Downloaded by guest on September 24, 2021 PHYSIOLOGY EDITORIAL EXPRESSION OF CONCERN 13217 Hyperglycemia in rodent models of type 2 diabetes requires insulin-resistant alpha cells Young Lee, Eric D. Berglund, Xinxin Yu, May-Yun Wang, Matthew R. Evans, Philipp E. Scherer, William L. Holland, 13241 Enhancing nuclear receptor-induced Maureen J. Charron, Michael G. Roth, and Roger H. Unger transcription requires nuclear motor and LSD1-dependent gene networking in POPULATION BIOLOGY interchromatin granules Qidong Hu, Young-Soo Kwon, Esperanza 13223 Demography, not inheritance, drives phenotypic change Nunez, Maria Dafne Cardamone, Kasey R. Hutt, in hunted bighorn sheep Kenneth A. Ohgi, Ivan Garcia-Bassets, David W. Rose, Lochran W. Traill, Susanne Schindler, and Tim Coulson Christopher K. Glass, Michael G. Rosenfeld, See Commentary on page 12964 and Xiang-Dong Fu

SUSTAINABILITY SCIENCE 13229 Highway proximity and black carbon from cookstoves as a risk factor for higher blood CORRECTION pressure in rural China Jill Baumgartner, Yuanxun Zhang, James J. Schauer, NEUROSCIENCE Wei Huang, Yuqin Wang, and Majid Ezzati 13241 When recognition memory is independent of hippocampal function SYSTEMS BIOLOGY Christine N. Smith, Annette Jeneson, Jennifer C. 13235 Surprisal analysis characterizes the free energy Frascino, C. Brock Kirwan, Ramona O. Hopkins, time course of cancer cells undergoing and Larry R. Squire epithelial-to-mesenchymal transition Sohila Zadran, Rameshkumar Arumugam, Harvey Herschman, Michael E. Phelps, and R. D. Levine ix Subscription Form

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