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Basic Research Paper

Intramembrane protease PARL defines a negative regulator of PINK1- and PARK2/Parkin-dependent mitophagy

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Pages 1484-1498 | Received 31 Jul 2014, Accepted 15 Jun 2015, Published online: 18 Sep 2015

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Jansson, Jonathan Jantsch, Sławomir Januszewski, Alagie Jassey, Steve Jean, Hélène Jeltsch-David, Pavla Jendelova, Andreas Jenny, Thomas E. Jensen, Niels Jessen, Jenna L. Jewell, Jing Ji, Lijun Jia, Rui Jia, Liwen Jiang, Qing Jiang, Richeng Jiang, Teng Jiang, Xuejun Jiang, Yu Jiang, Maria Jimenez-Sanchez, Eun-Jung Jin, Fengyan Jin, Hongchuan Jin, Li Jin, Luqi Jin, Meiyan Jin, Si Jin, Eun-Kyeong Jo, Carine Joffre, Terje Johansen, Gail V.W. Johnson, Simon A. Johnston, Eija Jokitalo, Mohit Kumar Jolly, Leo A.B. Joosten, Joaquin Jordan, Bertrand Joseph, Dianwen Ju, Jeong-Sun Ju, Jingfang Ju, Esmeralda Juárez, Delphine Judith, Gábor Juhász, Youngsoo Jun, Chang Hwa Jung, Sung-Chul Jung, Yong Keun Jung, Heinz Jungbluth, Johannes Jungverdorben, Steffen Just, Kai Kaarniranta, Allen Kaasik, Tomohiro Kabuta, Daniel Kaganovich, Alon Kahana, Renate Kain, Shinjo Kajimura, Maria Kalamvoki, Manjula Kalia, Danuta S. Kalinowski, Nina Kaludercic, Ioanna Kalvari, Joanna Kaminska, Vitaliy O. Kaminskyy, Hiromitsu Kanamori, Keizo Kanasaki, Chanhee Kang, Rui Kang, Sang Sun Kang, Senthilvelrajan Kaniyappan, Tomotake Kanki, Thirumala-Devi Kanneganti, Anumantha G. Kanthasamy, Arthi Kanthasamy, Marc Kantorow, Orsolya Kapuy, Michalis V. Karamouzis, Md. Razaul Karim, Parimal Karmakar, Rajesh G. Katare, Masaru Kato, Stefan H.E. Kaufmann, Anu Kauppinen, Gur P. Kaushal, Susmita Kaushik, Kiyoshi Kawasaki, Kemal Kazan, Po-Yuan Ke, Damien J. Keating, Ursula Keber, John H. Kehrl, Kate E. Keller, Christian W. Keller, Jongsook Kim Kemper, Candia M. Kenific, Oliver Kepp, Stephanie Kermorgant, Andreas Kern, Robin Ketteler, Tom G. Keulers, Boris Khalfin, Hany Khalil, Bilon Khambu, Shahid Y. Khan, Vinoth Kumar Megraj Khandelwal, Rekha Khandia, Widuri Kho, Noopur V. Khobrekar, Sataree Khuansuwan, Mukhran Khundadze, Samuel A. Killackey, Dasol Kim, Deok Ryong Kim, Do-Hyung Kim, Dong-Eun Kim, Eun Young Kim, Eun-Kyoung Kim, Hak-Rim Kim, Hee-Sik Kim, Hyung-Ryong Kim, Jeong Hun Kim, Jin Kyung Kim, Jin-Hoi Kim, Joungmok Kim, Ju Hwan Kim, Keun Il Kim, Peter K. Kim, Seong-Jun Kim, Scot R. Kimball, Adi Kimchi, Alec C. Kimmelman, Tomonori Kimura, Matthew A. King, Kerri J. Kinghorn, Conan G. Kinsey, Vladimir Kirkin, Lorrie A. Kirshenbaum, Sergey L. Kiselev, Shuji Kishi, Katsuhiko Kitamoto, Yasushi Kitaoka, Kaio Kitazato, Richard N. Kitsis, Josef T. Kittler, Ole Kjaerulff, Peter S. Klein, Thomas Klopstock, Jochen Klucken, Helene Knævelsrud, Roland L. Knorr, Ben C.B. Ko, Fred Ko, Jiunn-Liang Ko, Hotaka Kobayashi, Satoru Kobayashi, Ina Koch, Jan C. Koch, Ulrich Koenig, Donat Kögel, Young Ho Koh, Masato Koike, Sepp D. Kohlwein, Nur M. Kocaturk, Masaaki Komatsu, Jeannette König, Toru Kono, Benjamin T. Kopp, Tamas Korcsmaros, Gözde Korkmaz, Viktor I. Korolchuk, Mónica Suárez Korsnes, Ali Koskela, Janaiah Kota, Yaichiro Kotake, Monica L. Kotler, Yanjun Kou, Michael I. Koukourakis, Evangelos Koustas, Attila L. Kovacs, Tibor Kovács, Daisuke Koya, Tomohiro Kozako, Claudine Kraft, Dimitri Krainc, Helmut Krämer, Anna D. Krasnodembskaya, Carole Kretz-Remy, Guido Kroemer, Nicholas T. Ktistakis, Kazuyuki Kuchitsu, Sabine Kuenen, Lars Kuerschner, Thomas Kukar, Ajay Kumar, Ashok Kumar, Deepak Kumar, Dhiraj Kumar, Sharad Kumar, Shinji Kume, Caroline Kumsta, Chanakya N. Kundu, Mondira Kundu, Ajaikumar B. Kunnumakkara, Lukasz Kurgan, Tatiana G. Kutateladze, Ozlem Kutlu, SeongAe Kwak, Ho Jeong Kwon, Taeg Kyu Kwon, Yong Tae Kwon, Irene Kyrmizi, Albert La Spada, Patrick Labonté, Sylvain Ladoire, Ilaria Laface, Frank Lafont, Diane C. Lagace, Vikramjit Lahiri, Zhibing Lai, Angela S. Laird, Aparna Lakkaraju, Trond Lamark, Sheng-Hui Lan, Ane Landajuela, Darius J. R. Lane, Jon D. Lane, Charles H. Lang, Carsten Lange, Ülo Langel, Rupert Langer, Pierre Lapaquette, Jocelyn Laporte, Nicholas F. LaRusso, Isabel Lastres-Becker, Wilson Chun Yu Lau, Gordon W. Laurie, Sergio Lavandero, Betty Yuen Kwan Law, Helen Ka-wai Law, Rob Layfield, Weidong Le, Herve Le Stunff, Alexandre Y. Leary, Jean-Jacques Lebrun, Lionel Y.W. Leck, Jean-Philippe Leduc-Gaudet, Changwook Lee, Chung-Pei Lee, Da-Hye Lee, Edward B. Lee, Erinna F. Lee, Gyun Min Lee, He-Jin Lee, Heung Kyu Lee, Jae Man Lee, Jason S. Lee, Jin-A Lee, Joo-Yong Lee, Jun Hee Lee, Michael Lee, Min Goo Lee, Min Jae Lee, Myung-Shik Lee, Sang Yoon Lee, Seung-Jae Lee, Stella Y. Lee, Sung Bae Lee, Won Hee Lee, Ying-Ray Lee, Yong-ho Lee, Youngil Lee, Christophe Lefebvre, Renaud Legouis, Yu L. Lei, Yuchen Lei, Sergey Leikin, Gerd Leitinger, Leticia Lemus, Shuilong Leng, Olivia Lenoir, Guido Lenz, Heinz Josef Lenz, Paola Lenzi, Yolanda León, Andréia M. Leopoldino, Christoph Leschczyk, Stina Leskelä, Elisabeth Letellier, Chi-Ting Leung, Po Sing Leung, Jeremy S. Leventhal, Beth Levine, Patrick A. Lewis, Klaus Ley, Bin Li, Da-Qiang Li, Jianming Li, Jing Li, Jiong Li, Ke Li, Liwu Li, Mei Li, Min Li, Min Li, Ming Li, Mingchuan Li, Pin-Lan Li, Ming-Qing Li, Qing Li, Sheng Li, Tiangang Li, Wei Li, Wenming Li, Xue Li, Yi-Ping Li, Yuan Li, Zhiqiang Li, Zhiyong Li, Zhiyuan Li, Jiqin Lian, Chengyu Liang, Qiangrong Liang, Weicheng Liang, Yongheng Liang, YongTian Liang, Guanghong Liao, Lujian Liao, Mingzhi Liao, Yung-Feng Liao, Mariangela Librizzi, Pearl P. Y. Lie, Mary A. Lilly, Hyunjung J. Lim, Thania R.R. Lima, Federica Limana, Chao Lin, Chih-Wen Lin, Dar-Shong Lin, Fu-Cheng Lin, Jiandie D. Lin, Kurt M. Lin, Kwang-Huei Lin, Liang-Tzung Lin, Pei-Hui Lin, Qiong Lin, Shaofeng Lin, Su-Ju Lin, Wenyu Lin, Xueying Lin, Yao-Xin Lin, Yee-Shin Lin, Rafael Linden, Paula Lindner, Shuo-Chien Ling, Paul Lingor, Amelia K. 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Major, Elena Makareeva, Fayaz Malik, Karthik Mallilankaraman, Walter Malorni, Alina Maloyan, Najiba Mammadova, Gene Chi Wai Man, Federico Manai, Joseph D. Mancias, Eva-Maria Mandelkow, Michael A. Mandell, Angelo A. Manfredi, Masoud H. Manjili, Ravi Manjithaya, Patricio Manque, Bella B. Manshian, Raquel Manzano, Claudia Manzoni, Kai Mao, Cinzia Marchese, Sandrine Marchetti, Anna Maria Marconi, Fabrizio Marcucci, Stefania Mardente, Olga A. Mareninova, Marta Margeta, Muriel Mari, Sara Marinelli, Oliviero Marinelli, Guillermo Mariño, Sofia Mariotto, Richard S. Marshall, Mark R. Marten, Sascha Martens, Alexandre P.J. Martin, Katie R. Martin, Sara Martin, Shaun Martin, Adrián Martín-Segura, Miguel A. Martín-Acebes, Inmaculada Martin-Burriel, Marcos Martin-Rincon, Paloma Martin-Sanz, José A. Martina, Wim Martinet, Aitor Martinez, Ana Martinez, Jennifer Martinez, Moises Martinez Velazquez, Nuria Martinez-Lopez, Marta Martinez-Vicente, Daniel O. Martins, Joilson O. Martins, Waleska K. 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Menon, Carol Mercer, Anne E. Mercier, Jean-Louis Mergny, Adalberto Merighi, Seth D. Merkley, Giuseppe Merla, Volker Meske, Ana Cecilia Mestre, Shree Padma Metur, Christian Meyer, Hemmo Meyer, Wenyi Mi, Jeanne Mialet-Perez, Junying Miao, Lucia Micale, Yasuo Miki, Enrico Milan, Małgorzata Milczarek, Dana L. Miller, Samuel I. Miller, Silke Miller, Steven W. Millward, Ira Milosevic, Elena A. Minina, Hamed Mirzaei, Hamid Reza Mirzaei, Mehdi Mirzaei, Amit Mishra, Nandita Mishra, Paras Kumar Mishra, Maja Misirkic Marjanovic, Roberta Misasi, Amit Misra, Gabriella Misso, Claire Mitchell, Geraldine Mitou, Tetsuji Miura, Shigeki Miyamoto, Makoto Miyazaki, Mitsunori Miyazaki, Taiga Miyazaki, Keisuke Miyazawa, Noboru Mizushima, Trine H. Mogensen, Baharia Mograbi, Reza Mohammadinejad, Yasir Mohamud, Abhishek Mohanty, Sipra Mohapatra, Torsten Möhlmann, Asif Mohmmed, Anna Moles, Kelle H. Moley, Maurizio Molinari, Vincenzo Mollace, Andreas Buch Møller, Bertrand Mollereau, Faustino Mollinedo, Costanza Montagna, Mervyn J. Monteiro, Andrea Montella, L. Ruth Montes, Barbara Montico, Vinod K. Mony, Giacomo Monzio Compagnoni, Michael N. Moore, Mohammad A. Moosavi, Ana L. Mora, Marina Mora, David Morales-Alamo, Rosario Moratalla, Paula I. Moreira, Elena Morelli, Sandra Moreno, Daniel Moreno-Blas, Viviana Moresi, Benjamin Morga, Alwena H. Morgan, Fabrice Morin, Hideaki Morishita, Orson L. Moritz, Mariko Moriyama, Yuji Moriyasu, Manuela Morleo, Eugenia Morselli, Jose F. Moruno-Manchon, Jorge Moscat, Serge Mostowy, Elisa Motori, Andrea Felinto Moura, Naima Moustaid-Moussa, Maria Mrakovcic, Gabriel Muciño-Hernández, Anupam Mukherjee, Subhadip Mukhopadhyay, Jean M. Mulcahy Levy, Victoriano Mulero, Sylviane Muller, Christian Münch, Ashok Munjal, Pura Munoz-Canoves, Teresa Muñoz-Galdeano, Christian Münz, Tomokazu Murakawa, Claudia Muratori, Brona M. Murphy, J. 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Nixon, Annalisa Nobili, Clevio Nobrega, Takeshi Noda, Uxía Nogueira-Recalde, Trevor M. Nolan, Ivan Nombela, Ivana Novak, Beatriz Novoa, Takashi Nozawa, Nobuyuki Nukina, Carmen Nussbaum-Krammer, Jesper Nylandsted, Tracey R. O’Donovan, Seónadh M. O’Leary, Eyleen J. O’Rourke, Mary P. O’Sullivan, Timothy E. O’Sullivan, Salvatore Oddo, Ina Oehme, Michinaga Ogawa, Eric Ogier-Denis, Margret H. Ogmundsdottir, Besim Ogretmen, Goo Taeg Oh, Seon-Hee Oh, Young J. Oh, Takashi Ohama, Yohei Ohashi, Masaki Ohmuraya, Vasileios Oikonomou, Rani Ojha, Koji Okamoto, Hitoshi Okazawa, Masahide Oku, Sara Oliván, Jorge M. A. Oliveira, Michael Ollmann, James A. Olzmann, Shakib Omari, M. Bishr Omary, Gizem Önal, Martin Ondrej, Sang-Bing Ong, Sang-Ging Ong, Anna Onnis, Juan A. Orellana, Sara Orellana-Muñoz, Maria Del Mar Ortega-Villaizan, Xilma R. Ortiz-Gonzalez, Elena Ortona, Heinz D. Osiewacz, Abdel-Hamid K. Osman, Rosario Osta, Marisa S. Otegui, Kinya Otsu, Christiane Ott, Luisa Ottobrini, Jing-hsiung James Ou, Tiago F. Outeiro, Inger Oynebraten, Melek Ozturk, Gilles Pagès, Susanta Pahari, Marta Pajares, Utpal B. Pajvani, Rituraj Pal, Simona Paladino, Nicolas Pallet, Michela Palmieri, Giuseppe Palmisano, Camilla Palumbo, Francesco Pampaloni, Lifeng Pan, Qingjun Pan, Wenliang Pan, Xin Pan, Ganna Panasyuk, Rahul Pandey, Udai B. Pandey, Vrajesh Pandya, Francesco Paneni, Shirley Y. Pang, Elisa Panzarini, Daniela L. Papademetrio, Elena Papaleo, Daniel Papinski, Diana Papp, Eun Chan Park, Hwan Tae Park, Ji-Man Park, Jong-In Park, Joon Tae Park, Junsoo Park, Sang Chul Park, Sang-Youel Park, Abraham H. Parola, Jan B. Parys, Adrien Pasquier, Benoit Pasquier, João F. Passos, Nunzia Pastore, Hemal H. Patel, Daniel Patschan, Sophie Pattingre, Gustavo Pedraza-Alva, Jose Pedraza-Chaverri, Zully Pedrozo, Gang Pei, Jianming Pei, Hadas Peled-Zehavi, Joaquín M. Pellegrini, Joffrey Pelletier, Miguel A. 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Arjuna Ratnayaka, Edward A. Ratovitski, Palaniyandi Ravanan, Gloria Ravegnini, Swapan K. Ray, Babak Razani, Vito Rebecca, Fulvio Reggiori, Anne Régnier-Vigouroux, Andreas S. Reichert, David Reigada, Jan H. Reiling, Theo Rein, Siegfried Reipert, Rokeya Sultana Rekha, Hongmei Ren, Jun Ren, Weichao Ren, Tristan Renault, Giorgia Renga, Karen Reue, Kim Rewitz, Bruna Ribeiro de Andrade Ramos, S. Amer Riazuddin, Teresa M. Ribeiro-Rodrigues, Jean-Ehrland Ricci, Romeo Ricci, Victoria Riccio, Des R. Richardson, Yasuko Rikihisa, Makarand V. Risbud, Ruth M. Risueño, Konstantinos Ritis, Salvatore Rizza, Rosario Rizzuto, Helen C. Roberts, Luke D. Roberts, Katherine J. Robinson, Maria Carmela Roccheri, Stephane Rocchi, George G. Rodney, Tiago Rodrigues, Vagner Ramon Rodrigues Silva, Amaia Rodriguez, Ruth Rodriguez-Barrueco, Nieves Rodriguez-Henche, Humberto Rodriguez-Rocha, Jeroen Roelofs, Robert S. Rogers, Vladimir V. Rogov, Ana I. Rojo, Krzysztof Rolka, Vanina Romanello, Luigina Romani, Alessandra Romano, Patricia S. Romano, David Romeo-Guitart, Luis C. Romero, Montserrat Romero, Joseph C. Roney, Christopher Rongo, Sante Roperto, Mathias T. Rosenfeldt, Philip Rosenstiel, Anne G. Rosenwald, Kevin A. Roth, Lynn Roth, Steven Roth, Kasper M.A. Rouschop, Benoit D. Roussel, Sophie Roux, Patrizia Rovere-Querini, Ajit Roy, Aurore Rozieres, Diego Ruano, David C. Rubinsztein, Maria P. Rubtsova, Klaus Ruckdeschel, Christoph Ruckenstuhl, Emil Rudolf, Rüdiger Rudolf, Alessandra Ruggieri, Avnika Ashok Ruparelia, Paola Rusmini, Ryan R. Russell, Gian Luigi Russo, Maria Russo, Rossella Russo, Oxana O. Ryabaya, Kevin M. Ryan, Kwon-Yul Ryu, Maria Sabater-Arcis, Ulka Sachdev, Michael Sacher, Carsten Sachse, Abhishek Sadhu, Junichi Sadoshima, Nathaniel Safren, Paul Saftig, Antonia P. Sagona, Gaurav Sahay, Amirhossein Sahebkar, Mustafa Sahin, Ozgur Sahin, Sumit Sahni, Nayuta Saito, Shigeru Saito, Tsunenori Saito, Ryohei Sakai, Yasuyoshi Sakai, Jun-Ichi Sakamaki, Kalle Saksela, Gloria Salazar, Anna Salazar-Degracia, Ghasem H. Salekdeh, Ashok K. Saluja, Belém Sampaio-Marques, Maria Cecilia Sanchez, Jose A. Sanchez-Alcazar, Victoria Sanchez-Vera, Vanessa Sancho-Shimizu, J. Thomas Sanderson, Marco Sandri, Stefano Santaguida, Laura Santambrogio, Magda M. Santana, Giorgio Santoni, Alberto Sanz, Pascual Sanz, Shweta Saran, Marco Sardiello, Timothy J. Sargeant, Apurva Sarin, Chinmoy Sarkar, Sovan Sarkar, Maria-Rosa Sarrias, Surajit Sarkar, Dipanka Tanu Sarmah, Jaakko Sarparanta, Aishwarya Sathyanarayan, Ranganayaki Sathyanarayanan, K. Matthew Scaglione, Francesca Scatozza, Liliana Schaefer, Zachary T. Schafer, Ulrich E. Schaible, Anthony H.V. Schapira, Michael Scharl, Hermann M. Schatzl, Catherine H. 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Xiaobin Wen, Lixin Tang, Ruqing Zhong, Lei Liu, Liang Chen & Hongfu Zhang. (2023) Role of Mitophagy in Regulating Intestinal Oxidative Damage. Antioxidants 12:2, pages 480.
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Nolan M. Breault, Danchen Wu, Asish Dasgupta, Kuang-Hueih Chen & Stephen L. Archer. (2023) Acquired disorders of mitochondrial metabolism and dynamics in pulmonary arterial hypertension. Frontiers in Cell and Developmental Biology 11.
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Olimpo García-Beltrán, Pamela J. Urrutia & Marco T. Núñez. (2023) On the Chemical and Biological Characteristics of Multifunctional Compounds for the Treatment of Parkinson’s Disease. Antioxidants 12:2, pages 214.
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Edita Poláchová, Kathrin Bach, Elena Heuten, Stancho Stanchev, Anežka Tichá, Philipp Lampe, Pavel Majer, Thomas Langer, Marius K. Lemberg & Kvido Stříšovský. (2022) Chemical Blockage of the Mitochondrial Rhomboid Protease PARL by Novel Ketoamide Inhibitors Reveals Its Role in PINK1/Parkin-Dependent Mitophagy. Journal of Medicinal Chemistry 66:1, pages 251-265.
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Prakash Priyadarshi Praharaj, Birija Sankar Patro & Sujit Kumar Bhutia. (2021) Dysregulation of mitophagy and mitochondrial homeostasis in cancer stem cells: Novel mechanism for anti‐cancer stem cell‐targeted cancer therapy. British Journal of Pharmacology 179:22, pages 5015-5035.
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Jyotsna Asthana & Bhupendra V. Shravage. (2022) Exploring therapeutic potential of mitophagy modulators using Drosophila models of Parkinson’s disease. Frontiers in Aging Neuroscience 14.
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Verena Siebert, Mara Silber, Elena Heuten, Claudia Muhle-Goll & Marius K. Lemberg. (2022) Cleavage of mitochondrial homeostasis regulator PGAM5 by the intramembrane protease PARL is governed by transmembrane helix dynamics and oligomeric state. Journal of Biological Chemistry 298:9, pages 102321.
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Yang Liu, Miao Wang, Xiao-Ou Hou & Li-Fang Hu. (2022) Roles of microglial mitophagy in neurological disorders. Frontiers in Aging Neuroscience 14.
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Jiahui Tang, Yehong Zhuo & Yiqing Li. (2021) Effects of Iron and Zinc on Mitochondria: Potential Mechanisms of Glaucomatous Injury. Frontiers in Cell and Developmental Biology 9.
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Yue Feng, Kazem Nouri & Aaron D. Schimmer. (2021) Mitochondrial ATP-Dependent Proteases—Biological Function and Potential Anti-Cancer Targets. Cancers 13:9, pages 2020.
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Shalini Mani, Geeta Swargiary & Radhika Chadha. (2021) Mitophagy impairment in neurodegenerative diseases: Pathogenesis and therapeutic interventions. Mitochondrion 57, pages 270-293.
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Rohan Gupta, Rashmi K. Ambasta & Pravir Kumar. 2021. Mitochondrial Dysfunction and Nanotherapeutics. Mitochondrial Dysfunction and Nanotherapeutics 139 178 .
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Hester A. Beard, Marta Barniol-Xicota, Jian Yang & Steven H. L. Verhelst. (2019) Discovery of Cellular Roles of Intramembrane Proteases. ACS Chemical Biology 14:11, pages 2372-2388.
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Dario Valdinocci, Rui F. Simões, Jaromira Kovarova, Teresa Cunha-Oliveira, Jiri Neuzil & Dean L. Pountney. (2019) Intracellular and Intercellular Mitochondrial Dynamics in Parkinson’s Disease. Frontiers in Neuroscience 13.
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Astha Jaiswal, Christian H. Hoerth, Ana M. Zúñiga Pereira & Holger Lorenz. (2019) Improved spatial resolution by induced live cell and organelle swelling in hypotonic solutions. Scientific Reports 9:1.
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Matteo Audano, Anja Schneider & Nico Mitro. (2018) Mitochondria, lysosomes, and dysfunction: their meaning in neurodegeneration. Journal of Neurochemistry 147:3, pages 291-309.
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Kun Ma, Haoyu Wu, Peng Li & Baixiang Li. (2018) LC3-II may mediate ATR-induced mitophagy in dopaminergic neurons through SQSTM1/p62 pathway. Acta Biochimica et Biophysica Sinica 50:10, pages 1047-1061.
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Joshua G. Jackson & Michael B. Robinson. (2017) Regulation of mitochondrial dynamics in astrocytes: Mechanisms, consequences, and unknowns. Glia 66:6, pages 1213-1234.
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Laura Vera-Ramirez, Suman K. Vodnala, Ryan Nini, Kent W. Hunter & Jeffrey E. Green. (2018) Autophagy promotes the survival of dormant breast cancer cells and metastatic tumour recurrence. Nature Communications 9:1.
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Justine Lebeau, T. Kelly Rainbolt & R. Luke Wiseman. 2018. Mitochondria and Longevity. Mitochondria and Longevity 79 128 .
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