July 17, 2007 ͉ vol. 104 ͉ no. 29 ͉ 11863–12228

Proceedings of the National Academy ofPNAS Sciences of the United States of America www.pnas.org Cover image: Methane-oxidizing bacteria (Methylosinus trichosporium OB3b) cluster on copper- doped glass. Methanotrophic bacteria suppress methane, a major greenhouse gas. Expression of the bacterial enzyme methane monooxygenase is regulated by copper. Solid-phase copper geochemistry determines whether the metal is available for use. See the article by Knapp et al. on pages 12040–12045. Image courtesy of Ezra Kulczycki. From the Cover

12040 Copper geochemistry and methanotrophs 11901 Fabricating complex nanoparticles 11957 Fast dynamics of supercoiled DNA 12151 Inhibiting a TB virulence factor 12175 Stem cells reduce primate Parkinson’s symptoms

Contents INAUGURAL ARTICLES 11874 Late Pleistocene and Holocene environmental history of the Iguala Valley, Central Balsas Watershed of Mexico THIS WEEK IN PNAS D. R. Piperno, J. E. Moreno, J. Iriarte, I. Holst, M. Lachniet, J. G. Jones, A. J. Ranere, and R. Castanzo ➜ 11863 In This Issue See Profile on page 11871 11882 A comparative analysis of frog early development Eugenia M. del Pino, Michael Venegas-Ferrı´n, Andre´s COMMENTARIES Romero-Carvajal, Paola Montenegro-Larrea, Natalia Sa´enz-Ponce, Iva´n M. Moya, Ingrid Alarco´n, Norihiro 11865 Developmental genomics of the most dangerous animal Sudou, Shinji Yamamoto, and Masanori Taira Matthew P. Scott ➜ See companion article on page 11304 in issue 27 PHYSICAL SCIENCES of volume 104

11867 Physiology versus pathology in Parkinson’s disease APPLIED PHYSICAL SCIENCES Ken Nakamura and Robert H. Edwards 11889 Dissecting biological ‘‘dark matter’’ with single-cell ➜ See companion article on page 11441 in issue 27 genetic analysis of rare and uncultivated TM7 of volume 104 microbes from the human mouth Yann Marcy, Cleber Ouverney, Elisabeth M. Bik, Tina 11869 Neural stem cells for Parkinson’s disease: To protect Lo¨sekann, Natalia Ivanova, Hector Garcia Martin, and repair Ernest Szeto, Darren Platt, Philip Hugenholtz, Paul R. Sanberg David A. Relman, and Stephen R. Quake ➜ See companion article on page 12175 PROFILE 11895 Electrochemical attosyringe Franc¸ois O. Laforge, James Carpino, Susan A. Rotenberg, and Michael V. Mirkin 11871 Profile of Dolores R. Piperno Tinsley H. Davis ENGINEERING ➜ See Inaugural Article on page 11874 11901 Making polymeric micro- and nanoparticles of complex shapes Julie A. Champion, Yogesh K. Katare, Freely available online through the PNAS open access option. and Samir Mitragotri

PNAS ͉ July 17, 2007 ͉ vol. 104 ͉ no. 29 ͉ iii–vi Downloaded by guest on September 30, 2021 12169 Retinotopic mapping of adult human visual cortex 11951 Directed can rapidly improve the activity with high-density diffuse optical tomography of chimeric assembly-line enzymes Benjamin W. Zeff, Brian R. White, Hamid Dehghani, Michael A. Fischbach, Jonathan R. Lai, Eric D. Bradley L. Schlaggar, and Joseph P. Culver Roche, Christopher T. Walsh, and David R. Liu

SOCIAL SCIENCES BIOPHYSICS 11957 Fast dynamics of supercoiled DNA revealed by single-molecule experiments ANTHROPOLOGY Aure´lienCrut, Daniel A. Koster, Ralf Seidel, 11874 Late Pleistocene and Holocene environmental history of Chris H. Wiggins, and Nynke H. Dekker the Iguala Valley, Central Balsas Watershed of Mexico D. R. Piperno, J. E. Moreno, J. Iriarte, I. Holst, M. Lachniet, 11963 The design and characterization of two proteins with J. G. Jones, A. J. Ranere, and R. Castanzo 88% sequence identity but different structure ➜ See Profile on page 11871 and function Patrick A. Alexander, Yanan He, Yihong Chen, 11905 Precolumbian use of chili peppers in the Valley John Orban, and Philip N. Bryan of Oaxaca, Mexico 11969 Identifying important structural characteristics of arsenic Linda Perry and Kent V. Flannery resistance proteins by using designed three-stranded coiled coils BIOLOGICAL SCIENCES Debra S. Touw, Christer E. Nordman, Jeanne A. Stuckey, and Vincent L. Pecoraro

ANTHROPOLOGY 11975 Substrate-dependent transmembrane signaling 11910 Congruence of molecules and morphology using in TonB-dependent transporters is not conserved a narrow allometric approach Miyeon Kim, Gail E. Fanucci, and David S. Cafiso Christopher C. Gilbert and James B. Rossie 11981 The mechanism of rate-limiting motions in enzyme function APPLIED BIOLOGICAL SCIENCES Eric D. Watt, Hiroko Shimada, Evgenii L. 11915 Antithrombogenic property of bone marrow Kovrigin, and J. Patrick Loria mesenchymal stem cells in nanofibrous vascular grafts 11987 Protein folding by zipping and assembly Craig K. Hashi, Yiqian Zhu, Guo-Yuan Yang, S. Banu Ozkan, G. Albert Wu, John D. William L. Young, Benjamin S. Hsiao, Karin Chodera, and Ken A. Dill Wang, Benjamin Chu, and Song Li 11993 Observation of sequential steps in the folding of intestinal fatty acid binding protein using BIOCHEMISTRY a slow folding mutant and 19F NMR 11921 Hot spots in prion protein for pathogenic conversion Hua Li and Carl Frieden Kazuo Kuwata, Noriyuki Nishida, Tomoharu Matsumoto, Yuji O. Kamatari, Junji Hosokawa-Muto, Kota Kodama, CELL Hironori K. Nakamura, Kiminori Kimura, Makoto ⌬ Kawasaki, Yuka Takakura, Susumu Shirabe, Jiro 11999 Np63 regulates thymic development through enhanced Takata, Yasufumi Kataoka, and Shigeru Katamine expression of FgfR2 and Jag2 Eleonora Candi, Alessandro Rufini, Alessandro Terrinoni, 11927 Discovery of antiandrogen activity of nonsteroidal Alessandro Giamboi-Miraglia, Anna Maria Lena, Roberto scaffolds of marketed drugs Mantovani, Richard Knight, and Gerry Melino W. H. Bisson, A. V. Cheltsov, N. Bruey-Sedano, B. Lin, 12005 Essential role for MFG-E8 as ligand for ␣v␤5 integrin J. Chen, N. Goldberger, L. T. May, A. Christopoulos, in diurnal retinal phagocytosis J. T. Dalton, P. M. Sexton, X.-K. Zhang, and R. Abagyan Emeline F. Nandrot, Monika Anand, Dena Almeida, Kamran Atabai, Dean Sheppard, and Silvia C. Finnemann 11933 Src phosphorylation of cortactin enhances actin assembly Shandiz Tehrani, Nenad Tomasevic, Scott Weed, 12011 Functional specialization of ␤-arrestin interactions Roman Sakowicz, and John A. Cooper revealed by proteomic analysis Kunhong Xiao, Daniel B. McClatchy, Arun K. Shukla, 11939 Structural consequences of disease-causing mutations Yang Zhao, Minyong Chen, Sudha K. Shenoy, in the ATRX-DNMT3-DNMT3L (ADD) domain John R. Yates III, and Robert J. Lefkowitz of the chromatin-associated protein ATRX Anthony Argentaro, Ji-Chun Yang, Lynda Chapman, 12017 AMP-activated protein kinase (AMPK) action in skeletal Monika S. Kowalczyk, Richard J. Gibbons, Douglas R. muscle via direct phosphorylation of PGC-1␣ Higgs, David Neuhaus, and Daniela Rhodes Sibylle Ja¨ger, Christoph Handschin, Julie St.-Pierre, and Bruce M. Spiegelman 11945 Packing contacts can mediate highly specific interactions between artificial transmembrane proteins 12023 Otopetrin 1 activation by purinergic nucleotides and the PDGF␤ receptor regulates intracellular calcium Jennifer B. Ptacek, Anne P. B. Edwards, Inna Hughes, Mitsuyoshi Saito, Paul H. Schlesinger, Lisa L. Freeman-Cook, and Daniel DiMaio and David M. Ornitz

iv ͉ www.pnas.org Downloaded by guest on September 30, 2021 DEVELOPMENTAL BIOLOGY 12081 Natural killer cells actively patrol peripheral lymph 11882 A comparative analysis of frog early development nodes forming stable conjugates to eliminate MHC-mismatched targets Eugenia M. del Pino, Michael Venegas-Ferrı´n, Andre´s Romero-Carvajal, Paola Montenegro-Larrea, Natalia Kym R. Garrod, Sindy H. Wei, Ian Parker, Sa´enz-Ponce, Iva´n M. Moya, Ingrid Alarco´n, Norihiro and Michael D. Cahalan ؉ Sudou, Shinji Yamamoto, and Masanori Taira 12087 Association of cervical cancer with the presence of CD4 regulatory T cells specific for human 12029 Vertebrate Ctr1 coordinates morphogenesis and papillomavirus antigens progenitor cell fate and regulates embryonic Sjoerd H. van der Burg, Sytse J. Piersma, Annemieke de Jong, stem cell differentiation Jeanette M. van der Hulst, Kitty M. C. Kwappenberg, Muriel Tomomi Haremaki, Stuart T. Fraser, Yien-Ming Kuo, van den Hende, Marij J. P. Welters, Jon J. Van Rood, Margaret H. Baron, and Daniel C. Weinstein Gert Jan Fleuren, Cornelis J. M. Melief, Gemma G. Kenter, and Rienk Offringa ENVIRONMENTAL SCIENCES 12093 Peripheral deletion of mature alloreactive B cells induced by costimulation blockade 11874 Late Pleistocene and Holocene environmental history of Yijin Li, Lianli Ma, Jikun Shen, and Anita S. Chong the Iguala Valley, Central Balsas Watershed of Mexico D. R. Piperno, J. E. Moreno, J. Iriarte, I. Holst, M. Lachniet, 12099 IL-6-dependent and -independent pathways in the J. G. Jones, A. J. Ranere, and R. Castanzo development of interleukin 17-producing T helper cells ➜ See Profile on page 11871 Akihiro Kimura, Tetsuji Naka, and Tadamitsu Kishimoto 12105 Akt1 and Akt2 are required for ␣␤ thymocyte survival 12035 Hurricanes benefit bleached corals and differentiation Derek P. Manzello, Marilyn Brandt, Tyler B. Smith, Diego Marisa M. Juntilla, Jessica A. Wofford, Morris J. Birnbaum, Lirman, James C. Hendee, and Richard S. Nemeth Jeffrey C. Rathmell, and Gary A. Koretzky

12040 Methane monooxygenase gene expression mediated MEDICAL SCIENCES by methanobactin in the presence of mineral copper sources 12111 Somatic loss of BRCA1 and p53 in mice induces Charles W. Knapp, David A. Fowle, Ezra Kulczycki, mammary tumors with features of human Jennifer A. Roberts, and David W. Graham BRCA1-mutated basal-like breast cancer Xiaoling Liu, Henne Holstege, Hanneke van der Gulden, Marcelle Treur-Mulder, John Zevenhoven, Arno Velds, EVOLUTION Ron M. Kerkhoven, Martin H. van Vliet, Lodewyk F. A. 12046 Poxviruses as possible vectors for horizontal transfer Wessels, Johannes L. Peterse, Anton Berns, and Jos Jonkers of retroposons from reptiles to mammals 12117 Selective induction of chemotherapy resistance of Oliver Piskurek and Norihiro Okada mammary tumors in a conditional mouse model for hereditary breast cancer 12052 Temporal patterns of genes in scientific publications Sven Rottenberg, Anders O. H. Nygren, Marina Pajic, Thomas Pfeiffer and Robert Hoffmann Fijs W. B. van Leeuwen, Ingrid van der Heijden, Koen van de Wetering, Xiaoling Liu, Karin E. de Visser, 12057 Genome-wide patterns of single-feature polymorphism Kenneth G. Gilhuijs, Olaf van Tellingen, Jan P. in Schouten, Jos Jonkers, and Piet Borst Justin O. Borevitz, Samuel P. Hazen, Todd P. Michael, Geoffrey P. Morris, Ivan R. Baxter, Tina T. Hu, 12123 Potent cross-reactive neutralization of SARS coronavirus Huaming Chen, Jonathan D. Werner, Magnus isolates by human monoclonal antibodies Nordborg, David E. Salt, Steve A. Kay, Joanne Zhongyu Zhu, Samitabh Chakraborti, Yuxian He, Chory, Detlef Weigel, Jonathan D. G. Jones, Anjeanette Roberts, Tim Sheahan, Xiaodong Xiao, and Joseph R. Ecker Lisa E. Hensley, Ponraj Prabakaran, Barry Rockx, Igor A. Sidorov, Davide Corti, Leatrice Vogel, Yang Feng, Jae-Ouk Kim, Lin-Fa Wang, Ralph Baric, GENETICS Antonio Lanzavecchia, Kristopher M. Curtis, 12063 A connector of two-component regulatory systems Gary J. Nabel, Kanta Subbarao, Shibo Jiang, promotes signal amplification and persistence and Dimiter S. Dimitrov of expression 12129 Aristolochic acid and the etiology of endemic Akinori Kato, Alexander Y. Mitrophanov, (Balkan) nephropathy and Eduardo A. Groisman Arthur P. Grollman, Shinya Shibutani, Masaaki Moriya, Frederick Miller, Lin Wu, Ute Moll, Naomi Suzuki, 12069 A typology of photoreceptor gene expression patterns Andrea Fernandes, Thomas Rosenquist, Zvonimir in the mouse Medverec, Krunoslav Jakovina, Branko Brdar, Joseph C. Corbo, Connie A. Myers, Karen A. Lawrence, Neda Slade, Robert J. Turesky, Angela K. Ashutosh P. Jadhav, and Constance L. Cepko Goodenough, Robert Rieger, Mato Vukelic´, and Bojan Jelakovic´ IMMUNOLOGY 12135 Telomere length is paternally inherited and is associated 12075 CCR6-dependent recruitment of blood phagocytes with parental lifespan is necessary for rapid CD4 T cell responses to local Omer T. Njajou, Richard M. Cawthon, Coleen M. Damcott, bacterial infection Shih-Hsuan Wu, Sandy Ott, Michael J. Garant, Rajesh Ravindran, Lori Rusch, Andrea Itano, Elizabeth H. Blackburn, Braxton D. Mitchell, Marc K. Jenkins, and Stephen J. McSorley Alan R. Shuldiner, and Wen-Chi Hsueh

PNAS ͉ July 17, 2007 ͉ vol. 104 ͉ no. 29 ͉ v Downloaded by guest on September 30, 2021 12140 Combinatorial protein therapy of angiogenic 12181 GluR7 is an essential subunit of presynaptic kainate and arteriogenic factors remarkably improves autoreceptors at hippocampal mossy fiber synapses collaterogenesis and cardiac function in pigs Paulo S. Pinheiro, David Perrais, Franc¸oise Coussen, Huixia Lu, Xinsheng Xu, Mei Zhang, Renhai Cao, Jacques Barhanin, Bernhard Bettler, Jeffrey R. Mann, Ebba Bråkenhielm, Changjiang Li, Huili Lin, Guihua Joa˜o O. Malva, Stephen F. Heinemann, and Christophe Mulle Yao, Huiwen Sun, Lihang Qi, Mengxiong Tang, 12187 Baseline brain activity fluctuations predict Hongyan Dai, Yanen Zhang, Runyi Su, Yanwen somatosensory perception in humans Bi, Yun Zhang, and Yihai Cao M. Boly, E. Balteau, C. Schnakers, C. Degueldre, G. Moonen, A. Luxen, C. Phillips, P. Peigneux, MICROBIOLOGY P. Maquet, and S. Laureys 11889 Dissecting biological ‘‘dark matter’’ with single-cell 12193 Large-scale reorganization of the tonotopic map genetic analysis of rare and uncultivated TM7 in mouse auditory midbrain revealed by MRI microbes from the human mouth Xin Yu, Dan H. Sanes, Orlando Aristizabal, Youssef Yann Marcy, Cleber Ouverney, Elisabeth M. Bik, Tina Zaim Wadghiri, and Daniel H. Turnbull Lo¨sekann, Natalia Ivanova, Hector Garcia Martin, Ernest Szeto, Darren Platt, Philip Hugenholtz, PHARMACOLOGY David A. Relman, and Stephen R. Quake 12199 Dimerization of the class A G protein-coupled neurotensin receptor NTS1 alters G protein interaction 12146 Deep-sea vent ␧-proteobacterial genomes provide Jim F. White, Justin Grodnitzky, John M. Louis, Loc B. Trinh, insights into emergence of pathogens Joseph Shiloach, Joanne Gutierrez, John K. Northup, Satoshi Nakagawa, Yoshihiro Takaki, Shigeru Shimamura, and Reinhard Grisshammer Anna-Louise Reysenbach, Ken Takai, and Koki Horikoshi

12151 Structural basis for the specific inhibition BIOLOGY of protein kinase G, a virulence factor 12205 Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function of Mycobacterium tuberculosis in the systemin-mediated defense response against Nicole Scherr, Srinivas Honnappa, Gabriele Kunz, herbivorous insects Philipp Mueller, Rajesh Jayachandran, Fritz Pramod Kaitheri Kandoth, Stefanie Ranf, Suchita S. Winkler, Jean Pieters, and Michel O. Steinmetz Pancholi, Sastry Jayanty, Michael D. Walla, Wayne Miller, Gregg A. Howe, David E. Lincoln, 12157 Infection and coaccumulation of tobacco mosaic virus and Johannes W. Stratmann proteins alter microRNA levels, correlating with symptom and plant development 12211 Structural modules for receptor dimerization in the A. A. Bazzini, H. E. Hopp, R. N. Beachy, and S. Asurmendi S-locus receptor kinase extracellular domain Sushma Naithani, Thanat Chookajorn, Daniel R. Ripoll, 12163 Interaction of herpes simplex virus RNase with VP16 and June B. Nasrallah and VP22 is required for the accumulation of the 12217 The receptor-like kinase SERK3/BAK1 is a central protein but not for accumulation of mRNA regulator of innate immunity in Brunella Taddeo, Maria Teresa Sciortino, Weiran Zhang, Antje Heese, Dagmar R. Hann, Selena Gimenez-Ibanez, and Bernard Roizman Alexandra M. E. Jones, Kai He, Jia Li, Julian I. Schroeder, Scott C. Peck, and John P. Rathjen NEUROSCIENCE PSYCHOLOGY 12169 Retinotopic mapping of adult human visual cortex with high-density diffuse optical tomography 12223 A sound element gets lost in perceptual competition Benjamin W. Zeff, Brian R. White, Hamid Dehghani, Barbara G. Shinn-Cunningham, Adrian K. C. Lee, Bradley L. Schlaggar, and Joseph P. Culver and Andrew J. Oxenham

12175 Behavioral improvement in a primate Parkinson’s model CORRECTION is associated with multiple homeostatic effects of human neural stem cells D. Eugene Redmond, Jr., Kimberly B. Bjugstad, Yang D. EVOLUTION Teng, Vaclav Ourednik, Jitka Ourednik, Dustin R. 12228 Increase in toxicity of an invasive weed after Wakeman, Xuejun H. Parsons, Rodolfo Gonzalez, reassociation with its coevolved herbivore Barbara C. Blanchard, Seung U. Kim, Zezong Gu, Arthur R. Zangerl and May R. Berenbaum Stuart A. Lipton, Eleni A. Markakis, Robert H. Roth, John D. Elsworth, John R. Sladek, Jr., vii–viii Author Index Richard L. Sidman, and Evan Y. Snyder ➜ See Commentary on page 11869 ix Subscription Form

vi ͉ www.pnas.org Downloaded by guest on September 30, 2021