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Nature reviews. Disease primers. 2021:7(1).DOI: 10.1038/s41572-021-00269-y

Alzheimer disease

Knopman, David S; Amieva, Helene; Petersen, Ronald C; Chételat, Gäel; Holtzman, David M; Hyman, Bradley T; Nixon, Ralph A; Jones, David T
Alzheimer disease (AD) is biologically defined by the presence of β-amyloid-containing plaques and tau-containing neurofibrillary tangles. AD is a genetic and sporadic neurodegenerative disease that causes an amnestic cognitive impairment in its prototypical presentation and non-amnestic cognitive impairment in its less common variants. AD is a common cause of cognitive impairment acquired in midlife and late-life but its clinical impact is modified by other neurodegenerative and cerebrovascular conditions. This Primer conceives of AD biology as the brain disorder that results from a complex interplay of loss of synaptic homeostasis and dysfunction in the highly interrelated endosomal/lysosomal clearance pathways in which the precursors, aggregated species and post-translationally modified products of Aβ and tau play important roles. Therapeutic endeavours are still struggling to find targets within this framework that substantially change the clinical course in persons with AD.
PMID: 33986301
ISSN: 2056-676x
CID: 4889382
Hippocampus. 2021:31(5):522-539.DOI: 10.1002/hipo.23314

Dorsal and ventral mossy cells differ in their axonal projections throughout the dentate gyrus of the mouse hippocampus

Botterill, Justin J; Gerencer, Kathleen J; Vinod, K Yaragudri; Alcantara-Gonzalez, David; Scharfman, Helen E
Glutamatergic hilar mossy cells (MCs) have axons that terminate both near and far from their cell body but stay within the DG, making synapses primarily in the molecular layer. The long-range axons are considered the primary projection, and extend throughout the DG ipsilateral to the soma, and project to the contralateral DG. The specificity of MC axons for the inner molecular layer (IML) has been considered to be a key characteristic of the DG. In the present study, we made the surprising finding that dorsal MC axons are an exception to this rule. We used two mouse lines that allow for Cre-dependent viral labeling of MCs and their axons: dopamine receptor D2 (Drd2-Cre) and calcitonin receptor-like receptor (Crlr-Cre). A single viral injection into the dorsal DG to label dorsal MCs resulted in labeling of MC axons in both the IML and middle molecular layer (MML). Interestingly, this broad termination of dorsal MC axons occurred throughout the septotemporal DG. In contrast, long-range axons of ventral MCs terminated in the IML, consistent with the literature. Taken together, these results suggest that dorsal and ventral MCs differ significantly in their axonal projections. Since MC projections in the ML are thought to terminate primarily on GCs, the results suggest a dorsal-ventral difference in MC activation of GCs. The surprising difference in dorsal and ventral MC projections should therefore be considered when evaluating dorsal-ventral differences in DG function.
PMID: 33600026
ISSN: 1098-1063
CID: 4787032
Cell reports. 2021:35(4).DOI: 10.1016/j.celrep.2021.109034

Post-Golgi carriers, not lysosomes, confer lysosomal properties to pre-degradative organelles in normal and dystrophic axons

Lie, Pearl P Y; Yang, Dun-Sheng; Stavrides, Philip; Goulbourne, Chris N; Zheng, Ping; Mohan, Panaiyur S; Cataldo, Anne M; Nixon, Ralph A
Lysosomal trafficking and maturation in neurons remain poorly understood and are unstudied in vivo despite high disease relevance. We generated neuron-specific transgenic mice to track vesicular CTSD acquisition, acidification, and traffic within the autophagic-lysosomal pathway in vivo, revealing that mature lysosomes are restricted from axons. Moreover, TGN-derived transport carriers (TCs), not lysosomes, supply lysosomal components to axonal organelles. Ultrastructurally distinctive TCs containing TGN and lysosomal markers enter axons, engaging autophagic vacuoles and late endosomes. This process is markedly upregulated in dystrophic axons of Alzheimer models. In cultured neurons, most axonal LAMP1 vesicles are weakly acidic TCs that shuttle lysosomal components bidirectionally, conferring limited degradative capability to retrograde organelles before they mature fully to lysosomes within perikarya. The minor LAMP1 subpopulation attaining robust acidification are retrograde Rab7+ endosomes/amphisomes, not lysosomes. Restricted lysosome entry into axons explains the unique lysosome distribution in neurons and their vulnerability toward neuritic dystrophy in disease.
PMID: 33910020
ISSN: 2211-1247
CID: 4853382
Nature communications. 2021:12(1).DOI: 10.1038/s41467-021-22003-8

Cerebellar Kv3.3 potassium channels activate TANK-binding kinase 1 to regulate trafficking of the cell survival protein Hax-1

Zhang, Yalan; Varela, Luis; Szigeti-Buck, Klara; Williams, Adam; Stoiljkovic, Milan; Šestan-Peša, Matija; Henao-Mejia, Jorge; D'Acunzo, Pasquale; Levy, Efrat; Flavell, Richard A; Horvath, Tamas L; Kaczmarek, Leonard K
Mutations in KCNC3, which encodes the Kv3.3 potassium channel, cause degeneration of the cerebellum, but exactly how the activity of an ion channel is linked to the survival of cerebellar neurons is not understood. Here, we report that Kv3.3 channels bind and stimulate Tank Binding Kinase 1 (TBK1), an enzyme that controls trafficking of membrane proteins into multivesicular bodies, and that this stimulation is greatly increased by a disease-causing Kv3.3 mutation. TBK1 activity is required for the binding of Kv3.3 to its auxiliary subunit Hax-1, which prevents channel inactivation with depolarization. Hax-1 is also an anti-apoptotic protein required for survival of cerebellar neurons. Overactivation of TBK1 by the mutant channel leads to the loss of Hax-1 by its accumulation in multivesicular bodies and lysosomes, and also stimulates exosome release from neurons. This process is coupled to activation of caspases and increased cell death. Our studies indicate that Kv3.3 channels are directly coupled to TBK1-dependent biochemical pathways that determine the trafficking of cellular constituents and neuronal survival.
PMID: 33741962
ISSN: 2041-1723
CID: 4836162
Journal of neuroscience. 2021:41(11):2475-2495.DOI: 10.1523/JNEUROSCI.1724-20.2021

Bidirectional regulation of cognitive and anxiety-like behaviors by dentate gyrus mossy cells in male and female mice

Botterill, Justin J; Vinod, K Yaragudri; Gerencer, Kathleen J; Teixeira, Cátia M; LaFrancois, John J; Scharfman, Helen E
The dentate gyrus (DG) of the hippocampus is important for cognition and behavior. However, the circuits underlying these functions are unclear. DG mossy cells (MCs) are potentially important because of their excitatory synapses on the primary cell type, granule cells (GCs). However, MCs also activate GABAergic neurons which inhibit GCs. We used viral delivery of Designer Receptors Exclusively Activated by Designer Drugs (DREADDs) in mice to implement a gain- and loss of function study of MCs in diverse behaviors. Using this approach, manipulations of MCs could bidirectionally regulate behavior. The results suggest that inhibiting MCs can reduce anxiety-like behavior and improve cognitive performance. However, not all cognitive or anxiety-related behaviors were influenced, suggesting specific roles of MCs in some but not all types of cognition and anxiety. Notably, several behaviors showed sex-specific effects, with females often showing more pronounced effects than the males. We also used the immediate early gene c-Fos to address whether DREADDs bidirectionally regulated MC or GC activity. We confirmed excitatory DREADDs increased MC c-Fos. However, there was no change in GC c-Fos, consistent with MC activation leading to GABAergic inhibition of GCs. In contrast, inhibitory DREADDs led to a large increase in GC c-Fos, consistent with a reduction in MC excitation of GABAergic neurons, and reduced inhibition of GCs. Taken together, these results suggest that MCs regulate anxiety and cognition in specific ways. We also raise the possibility that cognitive performance may be improved by reducing anxiety.SIGNIFICANCE STATEMENT: The dentate gyrus (DG) has many important cognitive roles as well as being associated with affective behavior. This study addressed how a glutamatergic DG cell type called mossy cells (MCs) contributes to diverse behaviors, which is timely because it is known that MCs regulate the activity of the primary DG cell type, granule cells (GCs), but how MC activity influences behavior is unclear. We show, surprisingly, that activating MCs can lead to adverse behavioral outcomes, and inhibiting MCs have an opposite effect. Importantly, the results appeared to be task-dependent and showed that testing both sexes was important. Additional experiments indicated what MC and GC circuitry was involved. Taken together, the results suggest how MCs influence behaviors that involve the DG.
PMID: 33472828
ISSN: 1529-2401
CID: 4760652
Autophagy. 2021:1-382.DOI: 10.1080/15548627.2020.1797280

Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition)

Klionsky, Daniel J; Abdel-Aziz, Amal Kamal; Abdelfatah, Sara; Abdellatif, Mahmoud; Abdoli, Asghar; Abel, Steffen; Abeliovich, Hagai; Abildgaard, Marie H; Abudu, Yakubu Princely; Acevedo-Arozena, Abraham; Adamopoulos, Iannis E; Adeli, Khosrow; Adolph, Timon E; Adornetto, Annagrazia; Aflaki, Elma; Agam, Galila; Agarwal, Anupam; Aggarwal, Bharat B; Agnello, Maria; Agostinis, Patrizia; Agrewala, Javed N; Agrotis, Alexander; Aguilar, Patricia V; Ahmad, S Tariq; Ahmed, Zubair M; Ahumada-Castro, Ulises; Aits, Sonja; Aizawa, Shu; Akkoc, Yunus; Akoumianaki, Tonia; Akpinar, Hafize Aysin; Al-Abd, Ahmed M; Al-Akra, Lina; Al-Gharaibeh, Abeer; Alaoui-Jamali, Moulay A; Alberti, Simon; Alcocer-Gómez, Elísabet; Alessandri, Cristiano; Ali, Muhammad; Alim Al-Bari, M Abdul; Aliwaini, Saeb; Alizadeh, Javad; Almacellas, Eugènia; Almasan, Alexandru; Alonso, Alicia; Alonso, Guillermo D; Altan-Bonnet, Nihal; Altieri, Dario C; Álvarez, Élida M C; Alves, Sara; Alves da Costa, Cristine; Alzaharna, Mazen M; Amadio, Marialaura; Amantini, Consuelo; Amaral, Cristina; Ambrosio, Susanna; Amer, Amal O; Ammanathan, Veena; An, Zhenyi; Andersen, Stig U; Andrabi, Shaida A; Andrade-Silva, Magaiver; Andres, Allen M; Angelini, Sabrina; Ann, David; Anozie, Uche C; Ansari, Mohammad Y; Antas, Pedro; Antebi, Adam; Antón, Zuriñe; Anwar, Tahira; Apetoh, Lionel; Apostolova, Nadezda; Araki, Toshiyuki; Araki, Yasuhiro; Arasaki, Kohei; Araújo, Wagner L; Araya, Jun; Arden, Catherine; Arévalo, Maria-Angeles; Arguelles, Sandro; Arias, Esperanza; Arikkath, Jyothi; Arimoto, Hirokazu; Ariosa, Aileen R; Armstrong-James, Darius; Arnauné-Pelloquin, Laetitia; Aroca, Angeles; Arroyo, Daniela S; Arsov, Ivica; Artero, Rubén; Asaro, Dalia Maria Lucia; Aschner, Michael; Ashrafizadeh, Milad; Ashur-Fabian, Osnat; Atanasov, Atanas G; Au, Alicia K; Auberger, Patrick; Auner, Holger W; Aurelian, Laure; Autelli, Riccardo; Avagliano, Laura; Ávalos, Yenniffer; Aveic, Sanja; Aveleira, Célia Alexandra; Avin-Wittenberg, Tamar; Aydin, Yucel; Ayton, Scott; Ayyadevara, Srinivas; Azzopardi, Maria; Baba, Misuzu; Backer, Jonathan M; Backues, Steven K; Bae, Dong-Hun; Bae, Ok-Nam; Bae, Soo Han; Baehrecke, Eric H; Baek, Ahruem; Baek, Seung-Hoon; Baek, Sung Hee; Bagetta, Giacinto; Bagniewska-Zadworna, Agnieszka; Bai, Hua; Bai, Jie; Bai, Xiyuan; Bai, Yidong; Bairagi, Nandadulal; Baksi, Shounak; Balbi, Teresa; Baldari, Cosima T; Balduini, Walter; Ballabio, Andrea; Ballester, Maria; Balazadeh, Salma; Balzan, Rena; Bandopadhyay, Rina; Banerjee, Sreeparna; Banerjee, Sulagna; Bánréti, Ágnes; Bao, Yan; Baptista, Mauricio S; Baracca, Alessandra; Barbati, Cristiana; Bargiela, Ariadna; Barilà, Daniela; Barlow, Peter G; Barmada, Sami J; Barreiro, Esther; Barreto, George E; Bartek, Jiri; Bartel, Bonnie; Bartolome, Alberto; Barve, Gaurav R; Basagoudanavar, Suresh H; Bassham, Diane C; Bast, Robert C; Basu, Alakananda; Batoko, Henri; Batten, Isabella; Baulieu, Etienne E; Baumgarner, Bradley L; Bayry, Jagadeesh; Beale, Rupert; Beau, Isabelle; Beaumatin, Florian; Bechara, Luiz R G; Beck, George R; Beers, Michael F; Begun, Jakob; Behrends, Christian; Behrens, Georg M N; Bei, Roberto; Bejarano, Eloy; Bel, Shai; Behl, Christian; Belaid, Amine; Belgareh-Touzé, Naïma; Bellarosa, Cristina; Belleudi, Francesca; Belló Pérez, Melissa; Bello-Morales, Raquel; Beltran, Jackeline Soares de Oliveira; Beltran, Sebastián; Benbrook, Doris Mangiaracina; Bendorius, Mykolas; Benitez, Bruno A; Benito-Cuesta, Irene; Bensalem, Julien; Berchtold, Martin W; Berezowska, Sabina; Bergamaschi, Daniele; Bergami, Matteo; Bergmann, Andreas; Berliocchi, Laura; Berlioz-Torrent, Clarisse; Bernard, Amélie; Berthoux, Lionel; Besirli, Cagri G; Besteiro, Sebastien; Betin, Virginie M; Beyaert, Rudi; Bezbradica, Jelena S; Bhaskar, Kiran; Bhatia-Kissova, Ingrid; Bhattacharya, Resham; Bhattacharya, Sujoy; Bhattacharyya, Shalmoli; Bhuiyan, Md Shenuarin; Bhutia, Sujit Kumar; Bi, Lanrong; Bi, Xiaolin; Biden, Trevor J; Bijian, Krikor; Billes, Viktor A; Binart, Nadine; Bincoletto, Claudia; Birgisdottir, Asa B; Bjorkoy, Geir; Blanco, Gonzalo; Blas-Garcia, Ana; Blasiak, Janusz; Blomgran, Robert; Blomgren, Klas; Blum, Janice S; Boada-Romero, Emilio; Boban, Mirta; Boesze-Battaglia, Kathleen; Boeuf, Philippe; Boland, Barry; Bomont, Pascale; Bonaldo, Paolo; Bonam, Srinivasa Reddy; Bonfili, Laura; Bonifacino, Juan S; Boone, Brian A; Bootman, Martin D; Bordi, Matteo; Borner, Christoph; Bornhauser, Beat C; Borthakur, Gautam; Bosch, Jürgen; Bose, Santanu; Botana, Luis M; Botas, Juan; Boulanger, Chantal M; Boulton, Michael E; Bourdenx, Mathieu; Bourgeois, Benjamin; Bourke, Nollaig M; Bousquet, Guilhem; Boya, Patricia; Bozhkov, Peter V; Bozi, Luiz H M; Bozkurt, Tolga O; Brackney, Doug E; Brandts, Christian H; Braun, Ralf J; Braus, Gerhard H; Bravo-Sagua, Roberto; Bravo-San Pedro, José M; Brest, Patrick; Bringer, Marie-Agnès; Briones-Herrera, Alfredo; Broaddus, V Courtney; Brodersen, Peter; Brodsky, Jeffrey L; Brody, Steven L; Bronson, Paola G; Bronstein, Jeff M; Brown, Carolyn N; Brown, Rhoderick E; Brum, Patricia C; Brumell, John H; Brunetti-Pierri, Nicola; Bruno, Daniele; Bryson-Richardson, Robert J; Bucci, Cecilia; Buchrieser, Carmen; Bueno, Marta; Buitrago-Molina, Laura Elisa; Buraschi, Simone; Buch, Shilpa; Buchan, J Ross; Buckingham, Erin M; Budak, Hikmet; Budini, Mauricio; Bultynck, Geert; Burada, Florin; Burgoyne, Joseph R; Burón, M Isabel; Bustos, Victor; Büttner, Sabrina; Butturini, Elena; Byrd, Aaron; Cabas, Isabel; Cabrera-Benitez, Sandra; Cadwell, Ken; Cai, Jingjing; Cai, Lu; Cai, Qian; Cairó, Montserrat; Calbet, Jose A; Caldwell, Guy A; Caldwell, Kim A; Call, Jarrod A; Calvani, Riccardo; Calvo, Ana C; Calvo-Rubio Barrera, Miguel; Camara, Niels Os; Camonis, Jacques H; Camougrand, Nadine; Campanella, Michelangelo; Campbell, Edward M; Campbell-Valois, François-Xavier; Campello, Silvia; Campesi, Ilaria; Campos, Juliane C; Camuzard, Olivier; Cancino, Jorge; Candido de Almeida, Danilo; Canesi, Laura; Caniggia, Isabella; Canonico, Barbara; Cantí, Carles; Cao, Bin; Caraglia, Michele; Caramés, Beatriz; Carchman, Evie H; Cardenal-Muñoz, Elena; Cardenas, Cesar; Cardenas, Luis; Cardoso, Sandra M; Carew, Jennifer S; Carle, Georges F; Carleton, Gillian; Carloni, Silvia; Carmona-Gutierrez, Didac; Carneiro, Leticia A; Carnevali, Oliana; Carosi, Julian M; Carra, Serena; Carrier, Alice; Carrier, Lucie; Carroll, Bernadette; Carter, A Brent; Carvalho, Andreia Neves; Casanova, Magali; Casas, Caty; Casas, Josefina; Cassioli, Chiara; Castillo, Eliseo F; Castillo, Karen; Castillo-Lluva, Sonia; Castoldi, Francesca; Castori, Marco; Castro, Ariel F; Castro-Caldas, Margarida; Castro-Hernandez, Javier; Castro-Obregon, Susana; Catz, Sergio D; Cavadas, Claudia; Cavaliere, Federica; Cavallini, Gabriella; Cavinato, Maria; Cayuela, Maria L; Cebollada Rica, Paula; Cecarini, Valentina; Cecconi, Francesco; Cechowska-Pasko, Marzanna; Cenci, Simone; Ceperuelo-Mallafré, Victòria; Cerqueira, João J; Cerutti, Janete M; Cervia, Davide; Cetintas, Vildan Bozok; Cetrullo, Silvia; Chae, Han-Jung; Chagin, Andrei S; Chai, Chee-Yin; Chakrabarti, Gopal; Chakrabarti, Oishee; Chakraborty, Tapas; Chakraborty, Trinad; Chami, Mounia; Chamilos, Georgios; Chan, David W; Chan, Edmond Y W; Chan, Edward D; Chan, H Y Edwin; Chan, Helen H; Chan, Hung; Chan, Matthew T V; Chan, Yau Sang; Chandra, Partha K; Chang, Chih-Peng; Chang, Chunmei; Chang, Hao-Chun; Chang, Kai; Chao, Jie; Chapman, Tracey; Charlet-Berguerand, Nicolas; Chatterjee, Samrat; Chaube, Shail K; Chaudhary, Anu; Chauhan, Santosh; Chaum, Edward; Checler, Frédéric; Cheetham, Michael E; Chen, Chang-Shi; Chen, Guang-Chao; Chen, Jian-Fu; Chen, Liam L; Chen, Leilei; Chen, Lin; Chen, Mingliang; Chen, Mu-Kuan; Chen, Ning; Chen, Quan; Chen, Ruey-Hwa; Chen, Shi; Chen, Wei; Chen, Weiqiang; Chen, Xin-Ming; Chen, Xiong-Wen; Chen, Xu; Chen, Yan; Chen, Ye-Guang; Chen, Yingyu; Chen, Yongqiang; Chen, Yu-Jen; Chen, Yue-Qin; Chen, Zhefan Stephen; Chen, Zhi; Chen, Zhi-Hua; Chen, Zhijian J; Chen, Zhixiang; Cheng, Hanhua; Cheng, Jun; Cheng, Shi-Yuan; Cheng, Wei; Cheng, Xiaodong; Cheng, Xiu-Tang; Cheng, Yiyun; Cheng, Zhiyong; Chen, Zhong; Cheong, Heesun; Cheong, Jit Kong; Chernyak, Boris V; Cherry, Sara; Cheung, Chi Fai Randy; Cheung, Chun Hei Antonio; Cheung, King-Ho; Chevet, Eric; Chi, Richard J; Chiang, Alan Kwok Shing; Chiaradonna, Ferdinando; Chiarelli, Roberto; Chiariello, Mario; Chica, Nathalia; Chiocca, Susanna; Chiong, Mario; Chiou, Shih-Hwa; Chiramel, Abhilash I; Chiurchiù, Valerio; Cho, Dong-Hyung; Choe, Seong-Kyu; Choi, Augustine M K; Choi, Mary E; Choudhury, Kamalika Roy; Chow, Norman S; Chu, Charleen T; Chua, Jason P; Chua, John Jia En; Chung, Hyewon; Chung, Kin Pan; Chung, Seockhoon; Chung, So-Hyang; Chung, Yuen-Li; Cianfanelli, Valentina; Ciechomska, Iwona A; Cifuentes, Mariana; Cinque, Laura; Cirak, Sebahattin; Cirone, Mara; Clague, Michael J; Clarke, Robert; Clementi, Emilio; Coccia, Eliana M; Codogno, Patrice; Cohen, Ehud; Cohen, Mickael M; Colasanti, Tania; Colasuonno, Fiorella; Colbert, Robert A; Colell, Anna; ÄŒolić, Miodrag; Coll, Nuria S; Collins, Mark O; Colombo, María I; Colón-Ramos, Daniel A; Combaret, Lydie; Comincini, Sergio; Cominetti, Márcia R; Consiglio, Antonella; Conte, Andrea; Conti, Fabrizio; Contu, Viorica Raluca; Cookson, Mark R; Coombs, Kevin M; Coppens, Isabelle; Corasaniti, Maria Tiziana; Corkery, Dale P; Cordes, Nils; Cortese, Katia; Costa, Maria do Carmo; Costantino, Sarah; Costelli, Paola; Coto-Montes, Ana; Crack, Peter J; Crespo, Jose L; Criollo, Alfredo; Crippa, Valeria; Cristofani, Riccardo; Csizmadia, Tamas; Cuadrado, Antonio; Cui, Bing; Cui, Jun; Cui, Yixian; Cui, Yong; Culetto, Emmanuel; Cumino, Andrea C; Cybulsky, Andrey V; Czaja, Mark J; Czuczwar, Stanislaw J; D'Adamo, Stefania; D'Amelio, Marcello; D'Arcangelo, Daniela; D'Lugos, Andrew C; D'Orazi, Gabriella; da Silva, James A; Dafsari, Hormos Salimi; Dagda, Ruben K; Dagdas, Yasin; Daglia, Maria; Dai, Xiaoxia; Dai, Yun; Dai, Yuyuan; Dal Col, Jessica; Dalhaimer, Paul; Dalla Valle, Luisa; Dallenga, Tobias; Dalmasso, Guillaume; Damme, Markus; Dando, Ilaria; Dantuma, Nico P; Darling, April L; Das, Hiranmoy; Dasarathy, Srinivasan; Dasari, Santosh K; Dash, Srikanta; Daumke, Oliver; Dauphinee, Adrian N; Davies, Jeffrey S; Dávila, Valeria A; Davis, Roger J; Davis, Tanja; Dayalan Naidu, Sharadha; De Amicis, Francesca; De Bosscher, Karolien; De Felice, Francesca; De Franceschi, Lucia; De Leonibus, Chiara; de Mattos Barbosa, Mayara G; De Meyer, Guido R Y; De Milito, Angelo; De Nunzio, Cosimo; De Palma, Clara; De Santi, Mauro; De Virgilio, Claudio; De Zio, Daniela; Debnath, Jayanta; DeBosch, Brian J; Decuypere, Jean-Paul; Deehan, Mark A; Deflorian, Gianluca; DeGregori, James; Dehay, Benjamin; Del Rio, Gabriel; Delaney, Joe R; Delbridge, Lea M D; Delorme-Axford, Elizabeth; Delpino, M Victoria; Demarchi, Francesca; Dembitz, Vilma; Demers, Nicholas D; Deng, Hongbin; Deng, Zhiqiang; Dengjel, Joern; Dent, Paul; Denton, Donna; DePamphilis, Melvin L; Der, Channing J; Deretic, Vojo; Descoteaux, Albert; Devis, Laura; Devkota, Sushil; Devuyst, Olivier; Dewson, Grant; Dharmasivam, Mahendiran; Dhiman, Rohan; di Bernardo, Diego; Di Cristina, Manlio; Di Domenico, Fabio; Di Fazio, Pietro; Di Fonzo, Alessio; Di Guardo, Giovanni; Di Guglielmo, Gianni M; Di Leo, Luca; Di Malta, Chiara; Di Nardo, Alessia; Di Rienzo, Martina; Di Sano, Federica; Diallinas, George; Diao, Jiajie; Diaz-Araya, Guillermo; Díaz-Laviada, Inés; Dickinson, Jared M; Diederich, Marc; Dieudé, Mélanie; Dikic, Ivan; Ding, Shiping; Ding, Wen-Xing; Dini, Luciana; Dinić, Jelena; Dinic, Miroslav; Dinkova-Kostova, Albena T; Dionne, Marc S; Distler, Jörg H W; Diwan, Abhinav; Dixon, Ian M C; Djavaheri-Mergny, Mojgan; Dobrinski, Ina; Dobrovinskaya, Oxana; Dobrowolski, Radek; Dobson, Renwick C J; Đokić, Jelena; Dokmeci Emre, Serap; Donadelli, Massimo; Dong, Bo; Dong, Xiaonan; Dong, Zhiwu; Dorn Ii, Gerald W; Dotsch, Volker; Dou, Huan; Dou, Juan; Dowaidar, Moataz; Dridi, Sami; Drucker, Liat; Du, Ailian; Du, Caigan; Du, Guangwei; Du, Hai-Ning; Du, Li-Lin; du Toit, André; Duan, Shao-Bin; Duan, Xiaoqiong; Duarte, Sónia P; Dubrovska, Anna; Dunlop, Elaine A; Dupont, Nicolas; Durán, Raúl V; Dwarakanath, Bilikere S; Dyshlovoy, Sergey A; Ebrahimi-Fakhari, Darius; Eckhart, Leopold; Edelstein, Charles L; Efferth, Thomas; Eftekharpour, Eftekhar; Eichinger, Ludwig; Eid, Nabil; Eisenberg, Tobias; Eissa, N Tony; Eissa, Sanaa; Ejarque, Miriam; El Andaloussi, Abdeljabar; El-Hage, Nazira; El-Naggar, Shahenda; Eleuteri, Anna Maria; El-Shafey, Eman S; Elgendy, Mohamed; Eliopoulos, Aristides G; Elizalde, María M; Elks, Philip M; Elsasser, Hans-Peter; Elsherbiny, Eslam S; Emerling, Brooke M; Emre, N C Tolga; Eng, Christina H; Engedal, Nikolai; Engelbrecht, Anna-Mart; Engelsen, Agnete S T; Enserink, Jorrit M; Escalante, Ricardo; Esclatine, Audrey; Escobar-Henriques, Mafalda; Eskelinen, Eeva-Liisa; Espert, Lucile; Eusebio, Makandjou-Ola; Fabrias, Gemma; Fabrizi, Cinzia; Facchiano, Antonio; Facchiano, Francesco; Fadeel, Bengt; Fader, Claudio; Faesen, Alex C; Fairlie, W Douglas; Falcó, Alberto; Falkenburger, Bjorn H; Fan, Daping; Fan, Jie; Fan, Yanbo; Fang, Evandro F; Fang, Yanshan; Fang, Yognqi; Fanto, Manolis; Farfel-Becker, Tamar; Faure, Mathias; Fazeli, Gholamreza; Fedele, Anthony O; Feldman, Arthur M; Feng, Du; Feng, Jiachun; Feng, Lifeng; Feng, Yibin; Feng, Yuchen; Feng, Wei; Fenz Araujo, Thais; Ferguson, Thomas A; Fernández, Álvaro F; Fernandez-Checa, Jose C; Fernández-Veledo, Sonia; Fernie, Alisdair R; Ferrante, Anthony W; Ferraresi, Alessandra; Ferrari, Merari F; Ferreira, Julio C B; Ferro-Novick, Susan; Figueras, Antonio; Filadi, Riccardo; Filigheddu, Nicoletta; Filippi-Chiela, Eduardo; Filomeni, Giuseppe; Fimia, Gian Maria; Fineschi, Vittorio; Finetti, Francesca; Finkbeiner, Steven; Fisher, Edward A; Fisher, Paul B; Flamigni, Flavio; Fliesler, Steven J; Flo, Trude H; Florance, Ida; Florey, Oliver; Florio, Tullio; Fodor, Erika; Follo, Carlo; Fon, Edward A; Forlino, Antonella; Fornai, Francesco; Fortini, Paola; Fracassi, Anna; Fraldi, Alessandro; Franco, Brunella; Franco, Rodrigo; Franconi, Flavia; Frankel, Lisa B; Friedman, Scott L; Fröhlich, Leopold F; Frühbeck, Gema; Fuentes, Jose M; Fujiki, Yukio; Fujita, Naonobu; Fujiwara, Yuuki; Fukuda, Mitsunori; Fulda, Simone; Furic, Luc; Furuya, Norihiko; Fusco, Carmela; Gack, Michaela U; Gaffke, Lidia; Galadari, Sehamuddin; Galasso, Alessia; Galindo, Maria F; Gallolu Kankanamalage, Sachith; Galluzzi, Lorenzo; Galy, Vincent; Gammoh, Noor; Gan, Boyi; Ganley, Ian G; Gao, Feng; Gao, Hui; Gao, Minghui; Gao, Ping; Gao, Shou-Jiang; Gao, Wentao; Gao, Xiaobo; Garcera, Ana; Garcia, Maria Noé; Garcia, Verónica E; García-Del Portillo, Francisco; Garcia-Escudero, Vega; Garcia-Garcia, Aracely; Garcia-Macia, Marina; García-Moreno, Diana; Garcia-Ruiz, Carmen; García-Sanz, Patricia; Garg, Abhishek D; Gargini, Ricardo; Garofalo, Tina; Garry, Robert F; Gassen, Nils C; Gatica, Damian; Ge, Liang; Ge, Wanzhong; Geiss-Friedlander, Ruth; Gelfi, Cecilia; Genschik, Pascal; Gentle, Ian E; Gerbino, Valeria; Gerhardt, Christoph; Germain, Kyla; Germain, Marc; Gewirtz, David A; Ghasemipour Afshar, Elham; Ghavami, Saeid; Ghigo, Alessandra; Ghosh, Manosij; Giamas, Georgios; Giampietri, Claudia; Giatromanolaki, Alexandra; Gibson, Gary E; Gibson, Spencer B; Ginet, Vanessa; Giniger, Edward; Giorgi, Carlotta; Girao, Henrique; Girardin, Stephen E; Giridharan, Mridhula; Giuliano, Sandy; Giulivi, Cecilia; Giuriato, Sylvie; Giustiniani, Julien; Gluschko, Alexander; Goder, Veit; Goginashvili, Alexander; Golab, Jakub; Goldstone, David C; Golebiewska, Anna; Gomes, Luciana R; Gomez, Rodrigo; Gómez-Sánchez, Rubén; Gomez-Puerto, Maria Catalina; Gomez-Sintes, Raquel; Gong, Qingqiu; Goni, Felix M; González-Gallego, Javier; Gonzalez-Hernandez, Tomas; Gonzalez-Polo, Rosa A; Gonzalez-Reyes, Jose A; González-Rodríguez, Patricia; Goping, Ing Swie; Gorbatyuk, Marina S; Gorbunov, Nikolai V; Görgülü, Kıvanç; Gorojod, Roxana M; Gorski, Sharon M; Goruppi, Sandro; Gotor, Cecilia; Gottlieb, Roberta A; Gozes, Illana; Gozuacik, Devrim; Graef, Martin; Gräler, Markus H; Granatiero, Veronica; Grasso, Daniel; Gray, Joshua P; Green, Douglas R; Greenhough, Alexander; Gregory, Stephen L; Griffin, Edward F; Grinstaff, Mark W; Gros, Frederic; Grose, Charles; Gross, Angelina S; Gruber, Florian; Grumati, Paolo; Grune, Tilman; Gu, Xueyan; Guan, Jun-Lin; Guardia, Carlos M; Guda, Kishore; Guerra, Flora; Guerri, Consuelo; Guha, Prasun; Guillén, Carlos; Gujar, Shashi; Gukovskaya, Anna; Gukovsky, Ilya; Gunst, Jan; Günther, Andreas; Guntur, Anyonya R; Guo, Chuanyong; Guo, Chun; Guo, Hongqing; Guo, Lian-Wang; Guo, Ming; Gupta, Pawan; Gupta, Shashi Kumar; Gupta, Swapnil; Gupta, Veer Bala; Gupta, Vivek; Gustafsson, Asa B; Gutterman, David D; H B, Ranjitha; Haapasalo, Annakaisa; Haber, James E; Hać, Aleksandra; Hadano, Shinji; Hafrén, Anders J; Haidar, Mansour; Hall, Belinda S; Halldén, Gunnel; Hamacher-Brady, Anne; Hamann, Andrea; Hamasaki, Maho; Han, Weidong; Hansen, Malene; Hanson, Phyllis I; Hao, Zijian; Harada, Masaru; Harhaji-Trajkovic, Ljubica; Hariharan, Nirmala; Haroon, Nigil; Harris, James; Hasegawa, Takafumi; Hasima Nagoor, Noor; Haspel, Jeffrey A; Haucke, Volker; Hawkins, Wayne D; Hay, Bruce A; Haynes, Cole M; Hayrabedyan, Soren B; Hays, Thomas S; He, Congcong; He, Qin; He, Rong-Rong; He, You-Wen; He, Yu-Ying; Heakal, Yasser; Heberle, Alexander M; Hejtmancik, J Fielding; Helgason, Gudmundur Vignir; Henkel, Vanessa; Herb, Marc; Hergovich, Alexander; Herman-Antosiewicz, Anna; Hernández, Agustín; Hernandez, Carlos; Hernandez-Diaz, Sergio; Hernandez-Gea, Virginia; Herpin, Amaury; Herreros, Judit; Hervás, Javier H; Hesselson, Daniel; Hetz, Claudio; Heussler, Volker T; Higuchi, Yujiro; Hilfiker, Sabine; Hill, Joseph A; Hlavacek, William S; Ho, Emmanuel A; Ho, Idy H T; Ho, Philip Wing-Lok; Ho, Shu-Leong; Ho, Wan Yun; Hobbs, G Aaron; Hochstrasser, Mark; Hoet, Peter H M; Hofius, Daniel; Hofman, Paul; Höhn, Annika; Holmberg, Carina I; Hombrebueno, Jose R; Yi-Ren Hong, Chang-Won Hong; Hooper, Lora V; Hoppe, Thorsten; Horos, Rastislav; Hoshida, Yujin; Hsin, I-Lun; Hsu, Hsin-Yun; Hu, Bing; Hu, Dong; Hu, Li-Fang; Hu, Ming Chang; Hu, Ronggui; Hu, Wei; Hu, Yu-Chen; Hu, Zhuo-Wei; Hua, Fang; Hua, Jinlian; Hua, Yingqi; Huan, Chongmin; Huang, Canhua; Huang, Chuanshu; Huang, Chuanxin; Huang, Chunling; Huang, Haishan; Huang, Kun; Huang, Michael L H; Huang, Rui; Huang, Shan; Huang, Tianzhi; Huang, Xing; Huang, Yuxiang Jack; Huber, Tobias B; Hubert, Virginie; Hubner, Christian A; Hughes, Stephanie M; Hughes, William E; Humbert, Magali; Hummer, Gerhard; Hurley, James H; Hussain, Sabah; Hussain, Salik; Hussey, Patrick J; Hutabarat, Martina; Hwang, Hui-Yun; Hwang, Seungmin; Ieni, Antonio; Ikeda, Fumiyo; Imagawa, Yusuke; Imai, Yuzuru; Imbriano, Carol; Imoto, Masaya; Inman, Denise M; Inoki, Ken; Iovanna, Juan; Iozzo, Renato V; Ippolito, Giuseppe; Irazoqui, Javier E; Iribarren, Pablo; Ishaq, Mohd; Ishikawa, Makoto; Ishimwe, Nestor; Isidoro, Ciro; Ismail, Nahed; Issazadeh-Navikas, Shohreh; Itakura, Eisuke; Ito, Daisuke; Ivankovic, Davor; Ivanova, SaÅ¡ka; Iyer, Anand Krishnan V; Izquierdo, José M; Izumi, Masanori; Jäättelä, Marja; Jabir, Majid Sakhi; Jackson, William T; Jacobo-Herrera, Nadia; Jacomin, Anne-Claire; Jacquin, Elise; Jadiya, Pooja; Jaeschke, Hartmut; Jagannath, Chinnaswamy; Jakobi, Arjen J; Jakobsson, Johan; Janji, Bassam; Jansen-Dürr, Pidder; Jansson, Patric J; Jantsch, Jonathan; Januszewski, SÅ‚awomir; Jassey, Alagie; Jean, Steve; Jeltsch-David, Hélène; Jendelova, Pavla; Jenny, Andreas; Jensen, Thomas E; Jessen, Niels; Jewell, Jenna L; Ji, Jing; Jia, Lijun; Jia, Rui; Jiang, Liwen; Jiang, Qing; Jiang, Richeng; Jiang, Teng; Jiang, Xuejun; Jiang, Yu; Jimenez-Sanchez, Maria; Jin, Eun-Jung; Jin, Fengyan; Jin, Hongchuan; Jin, Li; Jin, Luqi; Jin, Meiyan; Jin, Si; Jo, Eun-Kyeong; Joffre, Carine; Johansen, Terje; Johnson, Gail V W; Johnston, Simon A; Jokitalo, Eija; Jolly, Mohit Kumar; Joosten, Leo A B; Jordan, Joaquin; Joseph, Bertrand; Ju, Dianwen; Ju, Jeong-Sun; Ju, Jingfang; Juárez, Esmeralda; Judith, Delphine; Juhász, Gábor; Jun, Youngsoo; Jung, Chang Hwa; Jung, Sung-Chul; Jung, Yong Keun; Jungbluth, Heinz; Jungverdorben, Johannes; Just, Steffen; Kaarniranta, Kai; Kaasik, Allen; Kabuta, Tomohiro; Kaganovich, Daniel; Kahana, Alon; Kain, Renate; Kajimura, Shinjo; Kalamvoki, Maria; Kalia, Manjula; Kalinowski, Danuta S; Kaludercic, Nina; Kalvari, Ioanna; Kaminska, Joanna; Kaminskyy, Vitaliy O; Kanamori, Hiromitsu; Kanasaki, Keizo; Kang, Chanhee; Kang, Rui; Kang, Sang Sun; Kaniyappan, Senthilvelrajan; Kanki, Tomotake; Kanneganti, Thirumala-Devi; Kanthasamy, Anumantha G; Kanthasamy, Arthi; Kantorow, Marc; Kapuy, Orsolya; Karamouzis, Michalis V; Karim, Md Razaul; Karmakar, Parimal; Katare, Rajesh G; Kato, Masaru; Kaufmann, Stefan H E; Kauppinen, Anu; Kaushal, Gur P; Kaushik, Susmita; Kawasaki, Kiyoshi; Kazan, Kemal; Ke, Po-Yuan; Keating, Damien J; Keber, Ursula; Kehrl, John H; Keller, Kate E; Keller, Christian W; Kemper, Jongsook Kim; Kenific, Candia M; Kepp, Oliver; Kermorgant, Stephanie; Kern, Andreas; Ketteler, Robin; Keulers, Tom G; Khalfin, Boris; Khalil, Hany; Khambu, Bilon; Khan, Shahid Y; 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Nabissi, Massimo; Nagy, Péter; Nah, Jihoon; Nahimana, Aimable; Nakagawa, Ichiro; Nakamura, Ken; Nakatogawa, Hitoshi; Nandi, Shyam S; Nanjundan, Meera; Nanni, Monica; Napolitano, Gennaro; Nardacci, Roberta; Narita, Masashi; Nassif, Melissa; Nathan, Ilana; Natsumeda, Manabu; Naude, Ryno J; Naumann, Christin; Naveiras, Olaia; Navid, Fatemeh; Nawrocki, Steffan T; Nazarko, Taras Y; Nazio, Francesca; Negoita, Florentina; Neill, Thomas; Neisch, Amanda L; Neri, Luca M; Netea, Mihai G; Neubert, Patrick; Neufeld, Thomas P; Neumann, Dietbert; Neutzner, Albert; Newton, Phillip T; Ney, Paul A; Nezis, Ioannis P; Ng, Charlene C W; Ng, Tzi Bun; Nguyen, Hang T T; Nguyen, Long T; Ni, Hong-Min; Ní Cheallaigh, Clíona; Ni, Zhenhong; Nicolao, M Celeste; Nicoli, Francesco; Nieto-Diaz, Manuel; Nilsson, Per; Ning, Shunbin; Niranjan, Rituraj; Nishimune, Hiroshi; Niso-Santano, Mireia; Nixon, Ralph A; Nobili, Annalisa; Nobrega, Clevio; Noda, Takeshi; Nogueira-Recalde, Uxía; Nolan, Trevor M; Nombela, Ivan; Novak, Ivana; Novoa, Beatriz; Nozawa, Takashi; Nukina, Nobuyuki; Nussbaum-Krammer, Carmen; Nylandsted, Jesper; O'Donovan, Tracey R; O'Leary, Seónadh M; O'Rourke, Eyleen J; O'Sullivan, Mary P; O'Sullivan, Timothy E; Oddo, Salvatore; Oehme, Ina; Ogawa, Michinaga; Ogier-Denis, Eric; Ogmundsdottir, Margret H; Ogretmen, Besim; Oh, Goo Taeg; Oh, Seon-Hee; Oh, Young J; Ohama, Takashi; Ohashi, Yohei; Ohmuraya, Masaki; Oikonomou, Vasileios; Ojha, Rani; Okamoto, Koji; Okazawa, Hitoshi; Oku, Masahide; Oliván, Sara; Oliveira, Jorge M A; Ollmann, Michael; Olzmann, James A; Omari, Shakib; Omary, M Bishr; Önal, Gizem; Ondrej, Martin; Ong, Sang-Bing; Ong, Sang-Ging; Onnis, Anna; Orellana, Juan A; Orellana-Muñoz, Sara; Ortega-Villaizan, Maria Del Mar; Ortiz-Gonzalez, Xilma R; Ortona, Elena; Osiewacz, Heinz D; Osman, Abdel-Hamid K; Osta, Rosario; Otegui, Marisa S; Otsu, Kinya; Ott, Christiane; Ottobrini, Luisa; Ou, Jing-Hsiung James; Outeiro, Tiago F; Oynebraten, Inger; Ozturk, Melek; Pagès, Gilles; Pahari, Susanta; 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Reipert, Siegfried; Rekha, Rokeya Sultana; Ren, Hongmei; Ren, Jun; Ren, Weichao; Renault, Tristan; Renga, Giorgia; Reue, Karen; Rewitz, Kim; Ribeiro de Andrade Ramos, Bruna; Riazuddin, S Amer; Ribeiro-Rodrigues, Teresa M; Ricci, Jean-Ehrland; Ricci, Romeo; Riccio, Victoria; Richardson, Des R; Rikihisa, Yasuko; Risbud, Makarand V; Risueño, Ruth M; Ritis, Konstantinos; Rizza, Salvatore; Rizzuto, Rosario; Roberts, Helen C; Roberts, Luke D; Robinson, Katherine J; Roccheri, Maria Carmela; Rocchi, Stephane; Rodney, George G; Rodrigues, Tiago; Rodrigues Silva, Vagner Ramon; Rodriguez, Amaia; Rodriguez-Barrueco, Ruth; Rodriguez-Henche, Nieves; Rodriguez-Rocha, Humberto; Roelofs, Jeroen; Rogers, Robert S; Rogov, Vladimir V; Rojo, Ana I; Rolka, Krzysztof; Romanello, Vanina; Romani, Luigina; Romano, Alessandra; Romano, Patricia S; Romeo-Guitart, David; Romero, Luis C; Romero, Montserrat; Roney, Joseph C; Rongo, Christopher; Roperto, Sante; Rosenfeldt, Mathias T; Rosenstiel, Philip; Rosenwald, Anne G; Roth, Kevin A; Roth, Lynn; Roth, Steven; Rouschop, Kasper M A; Roussel, Benoit D; Roux, Sophie; Rovere-Querini, Patrizia; Roy, Ajit; Rozieres, Aurore; Ruano, Diego; Rubinsztein, David C; Rubtsova, Maria P; Ruckdeschel, Klaus; Ruckenstuhl, Christoph; Rudolf, Emil; Rudolf, Rüdiger; Ruggieri, Alessandra; Ruparelia, Avnika Ashok; Rusmini, Paola; Russell, Ryan R; Russo, Gian Luigi; Russo, Maria; Russo, Rossella; Ryabaya, Oxana O; Ryan, Kevin M; Ryu, Kwon-Yul; Sabater-Arcis, Maria; Sachdev, Ulka; Sacher, Michael; Sachse, Carsten; Sadhu, Abhishek; Sadoshima, Junichi; Safren, Nathaniel; Saftig, Paul; Sagona, Antonia P; Sahay, Gaurav; Sahebkar, Amirhossein; Sahin, Mustafa; Sahin, Ozgur; Sahni, Sumit; Saito, Nayuta; Saito, Shigeru; Saito, Tsunenori; Sakai, Ryohei; Sakai, Yasuyoshi; Sakamaki, Jun-Ichi; Saksela, Kalle; Salazar, Gloria; Salazar-Degracia, Anna; Salekdeh, Ghasem H; Saluja, Ashok K; Sampaio-Marques, Belém; Sanchez, Maria Cecilia; Sanchez-Alcazar, Jose A; Sanchez-Vera, Victoria; Sancho-Shimizu, Vanessa; 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Yang, Wei Yuan; Yang, Xiaoyong; Yang, Xuesong; Yang, Yi; Yang, Ying; Yao, Honghong; Yao, Shenggen; Yao, Xiaoqiang; Yao, Yong-Gang; Yao, Yong-Ming; Yasui, Takahiro; Yazdankhah, Meysam; Yen, Paul M; Yi, Cong; Yin, Xiao-Ming; Yin, Yanhai; Yin, Zhangyuan; Yin, Ziyi; Ying, Meidan; Ying, Zheng; Yip, Calvin K; Yiu, Stephanie Pei Tung; Yoo, Young H; Yoshida, Kiyotsugu; Yoshii, Saori R; Yoshimori, Tamotsu; Yousefi, Bahman; Yu, Boxuan; Yu, Haiyang; Yu, Jun; Yu, Jun; Yu, Li; Yu, Ming-Lung; Yu, Seong-Woon; Yu, Victor C; Yu, W Haung; Yu, Zhengping; Yu, Zhou; Yuan, Junying; Yuan, Ling-Qing; Yuan, Shilin; Yuan, Shyng-Shiou F; Yuan, Yanggang; Yuan, Zengqiang; Yue, Jianbo; Yue, Zhenyu; Yun, Jeanho; Yung, Raymond L; Zacks, David N; Zaffagnini, Gabriele; Zambelli, Vanessa O; Zanella, Isabella; Zang, Qun S; Zanivan, Sara; Zappavigna, Silvia; Zaragoza, Pilar; Zarbalis, Konstantinos S; Zarebkohan, Amir; Zarrouk, Amira; Zeitlin, Scott O; Zeng, Jialiu; Zeng, Ju-Deng; Žerovnik, Eva; Zhan, Lixuan; Zhang, Bin; Zhang, Donna D; Zhang, Hanlin; Zhang, Hong; Zhang, Hong; Zhang, Honghe; Zhang, Huafeng; Zhang, Huaye; Zhang, Hui; Zhang, Hui-Ling; Zhang, Jianbin; Zhang, Jianhua; Zhang, Jing-Pu; Zhang, Kalin Y B; Zhang, Leshuai W; Zhang, Lin; Zhang, Lisheng; Zhang, Lu; Zhang, Luoying; Zhang, Menghuan; Zhang, Peng; Zhang, Sheng; Zhang, Wei; Zhang, Xiangnan; Zhang, Xiao-Wei; Zhang, Xiaolei; Zhang, Xiaoyan; Zhang, Xin; Zhang, Xinxin; Zhang, Xu Dong; Zhang, Yang; Zhang, Yanjin; Zhang, Yi; Zhang, Ying-Dong; Zhang, Yingmei; Zhang, Yuan-Yuan; Zhang, Yuchen; Zhang, Zhe; Zhang, Zhengguang; Zhang, Zhibing; Zhang, Zhihai; Zhang, Zhiyong; Zhang, Zili; Zhao, Haobin; Zhao, Lei; Zhao, Shuang; Zhao, Tongbiao; Zhao, Xiao-Fan; Zhao, Ying; Zhao, Yongchao; Zhao, Yongliang; Zhao, Yuting; Zheng, Guoping; Zheng, Kai; Zheng, Ling; Zheng, Shizhong; Zheng, Xi-Long; Zheng, Yi; Zheng, Zu-Guo; Zhivotovsky, Boris; Zhong, Qing; Zhou, Ao; Zhou, Ben; Zhou, Cefan; Zhou, Gang; Zhou, Hao; Zhou, Hong; Zhou, Hongbo; Zhou, Jie; Zhou, Jing; Zhou, Jing; Zhou, Jiyong; Zhou, Kailiang; Zhou, Rongjia; Zhou, Xu-Jie; Zhou, Yanshuang; Zhou, Yinghong; Zhou, Yubin; Zhou, Zheng-Yu; Zhou, Zhou; Zhu, Binglin; Zhu, Changlian; Zhu, Guo-Qing; Zhu, Haining; Zhu, Hongxin; Zhu, Hua; Zhu, Wei-Guo; Zhu, Yanping; Zhu, Yushan; Zhuang, Haixia; Zhuang, Xiaohong; Zientara-Rytter, Katarzyna; Zimmermann, Christine M; Ziviani, Elena; Zoladek, Teresa; Zong, Wei-Xing; Zorov, Dmitry B; Zorzano, Antonio; Zou, Weiping; Zou, Zhen; Zou, Zhengzhi; Zuryn, Steven; Zwerschke, Werner; Brand-Saberi, Beate; Dong, X Charlie; Kenchappa, Chandra Shekar; Li, Zuguo; Lin, Yong; Oshima, Shigeru; Rong, Yueguang; Sluimer, Judith C; Stallings, Christina L; Tong, Chun-Kit
In 2008, we published the first set of guidelines for standardizing research in autophagy. Since then, this topic has received increasing attention, and many scientists have entered the field. Our knowledge base and relevant new technologies have also been expanding. Thus, it is important to formulate on a regular basis updated guidelines for monitoring autophagy in different organisms. Despite numerous reviews, there continues to be confusion regarding acceptable methods to evaluate autophagy, especially in multicellular eukaryotes. Here, we present a set of guidelines for investigators to select and interpret methods to examine autophagy and related processes, and for reviewers to provide realistic and reasonable critiques of reports that are focused on these processes. These guidelines are not meant to be a dogmatic set of rules, because the appropriateness of any assay largely depends on the question being asked and the system being used. Moreover, no individual assay is perfect for every situation, calling for the use of multiple techniques to properly monitor autophagy in each experimental setting. Finally, several core components of the autophagy machinery have been implicated in distinct autophagic processes (canonical and noncanonical autophagy), implying that genetic approaches to block autophagy should rely on targeting two or more autophagy-related genes that ideally participate in distinct steps of the pathway. Along similar lines, because multiple proteins involved in autophagy also regulate other cellular pathways including apoptosis, not all of them can be used as a specific marker for bona fide autophagic responses. Here, we critically discuss current methods of assessing autophagy and the information they can, or cannot, provide. Our ultimate goal is to encourage intellectual and technical innovation in the field.
PMID: 33634751
ISSN: 1554-8635
CID: 4800842
Science advances. 2021:7(7).DOI: 10.1126/sciadv.abe5085

Mitovesicles are a novel population of extracellular vesicles of mitochondrial origin altered in Down syndrome

D'Acunzo, Pasquale; Pérez-González, Rocío; Kim, Yohan; Hargash, Tal; Miller, Chelsea; Alldred, Melissa J; Erdjument-Bromage, Hediye; Penikalapati, Sai C; Pawlik, Monika; Saito, Mitsuo; Saito, Mariko; Ginsberg, Stephen D; Neubert, Thomas A; Goulbourne, Chris N; Levy, Efrat
Mitochondrial dysfunction is an established hallmark of aging and neurodegenerative disorders such as Down syndrome (DS) and Alzheimer's disease (AD). Using a high-resolution density gradient separation of extracellular vesicles (EVs) isolated from murine and human DS and diploid control brains, we identify and characterize a previously unknown population of double-membraned EVs containing multiple mitochondrial proteins distinct from previously described EV subtypes, including microvesicles and exosomes. We term these newly identified mitochondria-derived EVs "mitovesicles." We demonstrate that brain-derived mitovesicles contain a specific subset of mitochondrial constituents and that their levels and cargo are altered during pathophysiological processes where mitochondrial dysfunction occurs, including in DS. The development of a method for the selective isolation of mitovesicles paves the way for the characterization in vivo of biological processes connecting EV biology and mitochondria dynamics and for innovative therapeutic and diagnostic strategies.
PMID: 33579698
ISSN: 2375-2548
CID: 4786222
Neurobiology of disease. 2021.DOI: 10.1016/j.nbd.2021.105274

Early changes in synaptic and intrinsic properties of dentate gyrus granule cells in a mouse model of Alzheimer's disease neuropathology and atypical effects of the cholinergic antagonist atropine

Alcantara-Gonzalez, David; Chartampila, Elissavet; Criscuolo, Chiara; Scharfman, Helen E
It has been reported that hyperexcitability occurs in a subset of patients with Alzheimer's disease (AD) and hyperexcitability could contribute to the disease. Several studies have suggested that the hippocampal dentate gyrus (DG) may be an important area where hyperexcitability occurs. Therefore, we tested the hypothesis that the principal DG cell type, granule cells (GCs), would exhibit changes at the single-cell level which would be consistent with hyperexcitability and might help explain it. We used the Tg2576 mouse, where it has been shown that hyperexcitability is robust at 2-3 months of age. GCs from 2 to 3-month-old Tg2576 mice were compared to age-matched wild type (WT) mice. Effects of muscarinic cholinergic antagonism were tested because previously we found that Tg2576 mice exhibited hyperexcitability in vivo that was reduced by the muscarinic cholinergic antagonist atropine, counter to the dogma that in AD one needs to boost cholinergic function. The results showed that GCs from Tg2576 mice exhibited increased frequency of spontaneous excitatory postsynaptic potentials/currents (sEPSP/Cs) and reduced frequency of spontaneous inhibitory synaptic events (sIPSCs) relative to WT, increasing the excitation:inhibition (E:I) ratio. There was an inward NMDA receptor-dependent current that we defined here as a novel synaptic current (nsC) in Tg2576 mice because it was very weak in WT mice. Intrinsic properties were distinct in Tg2576 GCs relative to WT. In summary, GCs of the Tg2576 mouse exhibit early electrophysiological alterations that are consistent with increased synaptic excitation, reduced inhibition, and muscarinic cholinergic dysregulation. The data support previous suggestions that the DG contributes to hyperexcitability and there is cholinergic dysfunction early in life in AD mouse models.
PMID: 33484828
ISSN: 1095-953x
CID: 4766672
Autism research. 2021:14(1):29-45.DOI: 10.1002/aur.2418

CIM6P/IGF-2 Receptor Ligands Reverse Deficits in Angelman Syndrome Model Mice

Cruz, Emmanuel; Descalzi, Giannina; Steinmetz, Adam; Scharfman, Helen E; Katzman, Aaron; Alberini, Cristina M
Angelman syndrome (AS), a genetic disorder that primarily affects the nervous system, is characterized by delayed development, intellectual disability, severe speech impairment, and problems with movement and balance (ataxia). Most affected children also have recurrent seizures (epilepsy). No existing therapies are capable of comprehensively treating the deficits in AS; hence, there is an urgent need to identify new treatments. Here we show that insulin-like growth factor 2 (IGF-2) and mannose-6-phosphate (M6P), ligands of two independent binding sites of the cation-independent M6P/IGF-2 receptor (CIM6P/IGF-2R), reverse most major deficits of AS modeled in mice. Subcutaneous injection of IGF-2 or M6P in mice modeling AS restored cognitive impairments as assessed by measurements of contextual and recognition memories, motor deficits assessed by rotarod and hindlimb clasping, and working memory/flexibility measured by Y-maze. IGF-2 also corrected deficits in marble burying and significantly attenuated acoustically induced seizures. An observational battery of tests confirmed that neither ligand changed basic functions including physical characteristics, general behavioral responses, and sensory reflexes, indicating that they are relatively safe. Our data provide strong preclinical evidence that targeting CIM6P/IGF-2R is a promising approach for developing novel therapeutics for AS. LAY SUMMARY: There is no effective treatment for the neurodevelopmental disorder Angelman syndrome (AS). Using a validated AS mouse model, the Ube3am-/p+ , in this study we show that systemic administration of ligands of the cation independent mannose-6-phosphate receptor, also known as insulin-like growth factor 2 receptor (CIM6P/IGF-2R) reverses cognitive impairment, motor deficits, as well as seizures associated with AS. Thus, ligands that activate the CIM6P/IGF-2R may represent novel, potential therapeutic targets for AS.
PMID: 33108069
ISSN: 1939-3806
CID: 4652142
Frontiers in aging neuroscience. 2021:13.DOI: 10.3389/fnagi.2021.791044

Editorial: Down Syndrome, Neurodegeneration and Dementia [Editorial]

Mufson, Elliott J; Ginsberg, Stephen D; Ma, Tao; Ledreux, Aurélie; Perez, Sylvia E
PMCID:8715919
PMID: 34975462
ISSN: 1663-4365
CID: 5106782