User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Proteomics of muscle chronological ageing in post-menopausal women

Primary tabs

download
  • Open access
  • PDF
  • 3.22 M
Gueugneau, Marine [UCL] Coudy-Gandilhon, Cécile Gourbeyre, Ophélie Chambon, Christophe Combaret, Lydie Béchet, Daniel

Background: Muscle ageing contributes to both loss of functional autonomy and increased morbidity. Muscle atrophy accelerates after 50 years of age, but the mechanisms involved are complex and likely result from the alteration of a variety of interrelated functions. In order to better understand the molecular mechanisms underlying muscle chronological ageing in human, we have undertaken a top-down differential proteomic approach to identify novel biomarkers after the fifth decade of age. Results: Muscle samples were compared between adult (56 years) and old (78 years) post-menopausal women. In addition to total muscle extracts, low-ionic strength extracts were investigated to remove high abundance myofibrillar proteins and improve the detection of low abundance proteins. Two-dimensional gel electrophoreses with overlapping IPGs were used to improve the separation of muscle proteins. Overall, 1919 protein spots were matched between all individuals, 95 were differentially expressed and identified by mass spectrometry, and they corresponded to 67 different proteins. Our results suggested important modifications in cytosolic, mitochondrial and lipid energy metabolism, which may relate to dysfunctions in old muscle force generation. A fraction of the differentially expressed proteins were linked to the sarcomere and cytoskeleton (myosin light-chains, troponin T, ankyrin repeat domain-containing protein-2, vinculin, four and a half LIM domain protein-3), which may account for alterations in contractile properties. In line with muscle contraction, we also identified proteins related to calcium signal transduction (calsequestrin-1, sarcalumenin, myozenin-1, annexins). Muscle ageing was further characterized by the differential regulation of several proteins implicated in cytoprotection (catalase, peroxiredoxins), ion homeostasis (carbonic anhydrases, selenium-binding protein 1) and detoxification (aldo-keto reductases, aldehyde dehydrogenases). Notably, many of the differentially expressed proteins were central for proteostasis, including heat shock proteins and proteins involved in proteolysis (valosin-containing protein, proteasome subunit beta type-4, mitochondrial elongation factor-Tu). Conclusions: This study describes the most extensive proteomic analysis of muscle ageing in humans, and identified 34 new potential biomarkers. None of them were previously recognized as differentially expressed in old muscles, and each may represent a novel starting point to elucidate the mechanisms of muscle chronological ageing in humans

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2014
Language Anglais
Journal information "BMC Genomics" - Vol. 15, no.1, p. 1165 [1-25] (2014)
Peer reviewed yes
Publisher BioMed Central Ltd. ((United Kingdom) London)
e-issn 1471-2164
Publication status Publié
Affiliation UCL - SSS/IREC/EDIN - Pôle d'endocrinologie, diabète et nutrition
MESH Subject Aged ; Humans ; Lipid Metabolism ; Middle Aged ; Mitochondria ; Muscle, Skeletal ; Muscles ; Oxidative Stress ; Postmenopause ; Proteolysis ; Proteomics ; Aging ; Sarcomeres ; Sarcopenia ; Signal Transduction ; Transcriptome ; Biomarkers ; Blood Proteins ; Cytoplasm ; Cytoskeletal Proteins ; Cytotoxins ; Energy Metabolism ; Female
Keywords Ageing ; Biomarkers ; Human ; Proteomics ; Sarcopenia ; Skeletal muscle
Links
  1. Bijlsma A. Y., Meskers C. G. M., Ling C. H. Y., Narici M., Kurrle S. E., Cameron I. D., Westendorp R. G. J., Maier A. B., Defining sarcopenia: the impact of different diagnostic criteria on the prevalence of sarcopenia in a large middle aged cohort, 10.1007/s11357-012-9384-z
  2. Taekema D. G., Gussekloo J., Maier A. B., Westendorp R. G. J., de Craen A. J. M., Handgrip strength as a predictor of functional, psychological and social health. A prospective population-based study among the oldest old, 10.1093/ageing/afq022
  3. Szulc P., Munoz F., Marchand F., Chapurlat R., Delmas P. D., Rapid loss of appendicular skeletal muscle mass is associated with higher all-cause mortality in older men: the prospective MINOS study, 10.3945/ajcn.2009.28256
  4. Sayer A. A., Robinson S. M., Patel H. P., Shavlakadze T., Cooper C., Grounds M. D., New horizons in the pathogenesis, diagnosis and management of sarcopenia, 10.1093/ageing/afs191
  5. Wang Huijuan, Listrat Anne, Meunier Bruno, Gueugneau Marine, Coudy-Gandilhon Cécile, Combaret Lydie, Taillandier Daniel, Polge Cécile, Attaix Didier, Lethias Claire, Lee Kijoon, Goh Kheng Lim, Béchet Daniel, Apoptosis in capillary endothelial cells in ageing skeletal muscle, 10.1111/acel.12169
  6. Carosio Silvia, Berardinelli Maria Grazia, Aucello Michela, Musarò Antonio, Impact of ageing on muscle cell regeneration, 10.1016/j.arr.2009.08.001
  7. Narici M. V., Maffulli N., Sarcopenia: characteristics, mechanisms and functional significance, 10.1093/bmb/ldq008
  8. Petersen K. F., Mitochondrial Dysfunction in the Elderly: Possible Role in Insulin Resistance, 10.1126/science.1082889
  9. Short K. R., Bigelow M. L., Kahl J., Singh R., Coenen-Schimke J., Raghavakaimal S., Nair K. S., Decline in skeletal muscle mitochondrial function with aging in humans, 10.1073/pnas.0501559102
  10. Lee C., Gene Expression Profile of Aging and Its Retardation by Caloric Restriction, 10.1126/science.285.5432.1390
  11. Baraibar Martin A., Gueugneau Marine, Duguez Stephanie, Butler-Browne Gillian, Bechet Daniel, Friguet Bertrand, Expression and modification proteomics during skeletal muscle ageing, 10.1007/s10522-013-9426-7
  12. Capitanio Daniele, Vasso Michele, Fania Chiara, Moriggi Manuela, Viganò Agnese, Procacci Patrizia, Magnaghi Valerio, Gelfi Cecilia, Comparative proteomic profile of rat sciatic nerve and gastrocnemius muscle tissues in ageing by 2-D DIGE, 10.1002/pmic.200701162
  13. Doran Philip, O'Connell Kathleen, Gannon Joan, Kavanagh Marcella, Ohlendieck Kay, Opposite pathobiochemical fate of pyruvate kinase and adenylate kinase in aged rat skeletal muscle as revealed by proteomic DIGE analysis, 10.1002/pmic.200700475
  14. Gannon Joan, Doran Philip, Kirwan Anne, Ohlendieck Kay, Drastic increase of myosin light chain MLC-2 in senescent skeletal muscle indicates fast-to-slow fibre transition in sarcopenia of old age, 10.1016/j.ejcb.2009.06.004
  15. O'Connell Kathleen, Ohlendieck Kay, Proteomic DIGE analysis of the mitochondria-enriched fraction from aged rat skeletal muscle, 10.1002/pmic.200900472
  16. Gelfi Cecilia, Viganò Agnese, Ripamonti Marilena, Pontoglio Alessandro, Begum Shajna, Pellegrino Maria Antonietta, Grassi Bruno, Bottinelli Roberto, Wait Robin, Cerretelli Paolo, The Human Muscle Proteome in Aging, 10.1021/pr050414x
  17. Neti G., Novak S. M., Thompson V. F., Goll D. E., Properties of easily releasable myofilaments: are they the first step in myofibrillar protein turnover?, 10.1152/ajpcell.00022.2009
  18. Wei Bin, Jin J.-P., Troponin T isoforms and posttranscriptional modifications: Evolution, regulation and function, 10.1016/j.abb.2010.10.013
  19. Pallavicini Alberto, Kojić Snezana, Bean Camilla, Vainzof Mariz, Salamon Michela, Ievolella Chiara, Bortoletto Gladis, Pacchioni Beniamima, Zatz Mayana, Lanfranchi Gerolamo, Faulkner Georgine, Valle Giorgio, Characterization of Human Skeletal Muscle Ankrd2, 10.1006/bbrc.2001.5131
  20. Hayashi Chikako, Ono Yasuko, Doi Naoko, Kitamura Fujiko, Tagami Mai, Mineki Reiko, Arai Takao, Taguchi Hayao, Yanagida Mitsuaki, Hirner Stephanie, Labeit Dietmar, Labeit Siegfried, Sorimachi Hiroyuki, Multiple Molecular Interactions Implicate the Connectin/Titin N2A Region as a Modulating Scaffold for p94/Calpain 3 Activity in Skeletal Muscle, 10.1074/jbc.m708262200
  21. Belgrano Anna, Rakicevic Ljiljana, Mittempergher Lorenza, Campanaro Stefano, Martinelli Valentina C., Mouly Vincent, Valle Giorgio, Kojic Snezana, Faulkner Georgine, Multi-Tasking Role of the Mechanosensing Protein Ankrd2 in the Signaling Network of Striated Muscle, 10.1371/journal.pone.0025519
  22. Tsukamoto Yoshiyuki, Senda Takao, Nakano Toshiya, Nakada Chisato, Hida Takehiko, Ishiguro Naoko, Kondo Gento, Baba Takeshi, Sato Kenzo, Osaki Mitsuhiko, Mori Shigeo, Ito Hisao, Moriyama Masatsugu, Arpp, a New Homolog of Carp, Is Preferentially Expressed in Type 1 Skeletal Muscle Fibers and Is Markedly Induced by Denervation, 10.1038/labinvest.3780459
  23. Dreyer Hans C., Blanco Cesar E., Sattler Fred R., Schroeder E. Todd, Wiswell Robert A., Satellite cell numbers in young and older men 24 hours after eccentric exercise, 10.1002/mus.20461
  24. Sato Tsuneko, Akatsuka Hiromichi, Kito Kuniyoshi, Tokoro Yoshiro, Tauchi Hisashi, Kato Kenefusa, Age changes in size and number of muscle fibers in human minor pectoral muscle, 10.1016/0047-6374(84)90156-8
  25. Kosek D. J., Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanisms in young vs. older adults, 10.1152/japplphysiol.01474.2005
  26. Ervasti James M., Costameres: the Achilles' Heel of Herculean Muscle, 10.1074/jbc.r200021200
  27. Humphries Jonathan D., Wang Pengbo, Streuli Charles, Geiger Benny, Humphries Martin J., Ballestrem Christoph, Vinculin controls focal adhesion formation by direct interactions with talin and actin, 10.1083/jcb.200703036
  28. Coghill Imogen D., Brown Susan, Cottle Denny L., McGrath Meagan J., Robinson Paul A., Nandurkar Harshal H., Dyson Jennifer M., Mitchell Christina A., FHL3 Is an Actin-binding Protein That Regulates α-Actinin-mediated Actin Bundling : FHL3 LOCALIZES TO ACTIN STRESS FIBERS AND ENHANCES CELL SPREADING AND STRESS FIBER DISASSEMBLY, 10.1074/jbc.m213259200
  29. Samson Thomas, Smyth Neil, Janetzky Stefanie, Wendler Olaf, Müller Judith M., Schüle Roland, von der Mark Helga, von der Mark Klaus, Wixler Viktor, The LIM-only Proteins FHL2 and FHL3 Interact with α- and β-Subunits of the Muscle α7β1Integrin Receptor, 10.1074/jbc.m312894200
  30. Meeson Annette P, Shi Xiaozhong, Alexander Matthew S, Williams R S, Allen Ronald E, Jiang Nan, Adham Ibrahim M, Goetsch Sean C, Hammer Robert E, Garry Daniel J, Sox15 and Fhl3 transcriptionally coactivate Foxk1 and regulate myogenic progenitor cells, 10.1038/sj.emboj.7601635
  31. Wei Lan, Gallant Esther M., Dulhunty Angela F., Beard Nicole A., Junctin and triadin each activate skeletal ryanodine receptors but junctin alone mediates functional interactions with calsequestrin, 10.1016/j.biocel.2009.04.017
  32. Bellinger Andrew M., Mongillo Marco, Marks Andrew R., Stressed out: the skeletal muscle ryanodine receptor as a target of stress, 10.1172/jci34006
  33. Gehlert Sebastian, Bungartz Gerd, Willkomm Lena, Korkmaz Yüksel, Pfannkuche Kurt, Schiffer Thorsten, Bloch Wilhelm, Suhr Frank, Intense Resistance Exercise Induces Early and Transient Increases in Ryanodine Receptor 1 Phosphorylation in Human Skeletal Muscle, 10.1371/journal.pone.0049326
  34. Mahaney James E, Weis Christopher P, Grisham Charles M, Kutchai Howard, Antibodies against the 53 kDa glycoprotein inhibit the rotational dynamics of both the 53 kDa glycoprotein and the Ca2+-ATPase in the sarcoplasmic reticulum membrane, 10.1016/0005-2736(91)90411-z
  35. Ferrington Deborah A., Krainev Arkadi G., Bigelow Diana J., Altered Turnover of Calcium Regulatory Proteins of the Sarcoplasmic Reticulum in Aged Skeletal Muscle, 10.1074/jbc.273.10.5885
  36. O’Connell Kathleen, Gannon Joan, Doran Philip, Ohlendieck Kay, Reduced expression of sarcalumenin and related Ca2+-regulatory proteins in aged rat skeletal muscle, 10.1016/j.exger.2008.07.006
  37. Frey Norbert, Frank Derk, Lippl Stefanie, Kuhn Christian, Kögler Harald, Barrientos Tomasa, Rohr Claudia, Will Rainer, Müller Oliver J., Weiler Hartmut, Bassel-Duby Rhonda, Katus Hugo A., Olson Eric N., Calsarcin-2 deficiency increases exercise capacity in mice through calcineurin/NFAT activation, 10.1172/jci36277
  38. Bizzarro Valentina, Belvedere Raffaella, Dal Piaz Fabrizio, Parente Luca, Petrella Antonello, Annexin A1 Induces Skeletal Muscle Cell Migration Acting through Formyl Peptide Receptors, 10.1371/journal.pone.0048246
  39. Leikina Evgenia, Melikov Kamran, Sanyal Sarmistha, Verma Santosh K., Eun Bokkee, Gebert Claudia, Pfeifer Karl, Lizunov Vladimir A., Kozlov Michael M., Chernomordik Leonid V., Extracellular annexins and dynamin are important for sequential steps in myoblast fusion, 10.1083/jcb.201207012
  40. Wang Li, Dong ZhiWu, Huang Bin, Zhao BaoXiang, Wang Hua, Zhao Jing, Kung HsiangFu, Zhang ShangLi, Miao JunYing, Distinct patterns of autophagy evoked by two benzoxazine derivatives in vascular endothelial cells, 10.4161/auto.6.8.13508
  41. Board Philip G., Coggan Marjorie, Chelvanayagam Gareth, Easteal Simon, Jermiin Lars S., Schulte Gayle K., Danley Dennis E., Hoth Lise R., Griffor Matthew C., Kamath Ajith V., Rosner Michele H., Chrunyk Boris A., Perregaux David E., Gabel Christopher A., Geoghegan Kieran F., Pandit Jayvardhan, Identification, Characterization, and Crystal Structure of the Omega Class Glutathione Transferases, 10.1074/jbc.m001706200
  42. Dulhunty Angela, Gage Peter, Curtis Suzanne, Chelvanayagam Gareth, Board Philip, The Glutathione Transferase Structural Family Includes a Nuclear Chloride Channel and a Ryanodine Receptor Calcium Release Channel Modulator, 10.1074/jbc.m007874200
  43. Kelly T. J., Souza A. L., Clish C. B., Puigserver P., A Hypoxia-Induced Positive Feedback Loop Promotes Hypoxia-Inducible Factor 1  Stability through miR-210 Suppression of Glycerol-3-Phosphate Dehydrogenase 1-Like, 10.1128/mcb.01242-10
  44. Orosz Ferenc, Oláh Judit, Ovádi Judit, Triosephosphate isomerase deficiency: New insights into an enigmatic disease, 10.1016/j.bbadis.2009.09.012
  45. Hipkiss Alan R., Energy metabolism and ageing regulation: Metabolically driven deamidation of triosephosphate isomerase may contribute to proteostatic dysfunction, 10.1016/j.arr.2011.05.003
  46. Fischer Heléne, Gustafsson Thomas, Sundberg Carl Johan, Norrbom Jessica, Ekman Marianne, Johansson Olle, Jansson Eva, Fatty acid binding protein 4 in human skeletal muscle, 10.1016/j.bbrc.2006.05.083
  47. Luiken J. J. F. P., Koonen D. P. Y., Coumans W. A., Pelsers M. M. A. L., Binas B., Bonen A., Glatz J. F. C., Long-chain fatty acid uptake by skeletal muscle is impaired in homozygous, but not heterozygous, heart-type-FABP null mice, 10.1007/s11745-003-1089-6
  48. Erbay Ebru, Babaev Vladimir R, Mayers Jared R, Makowski Liza, Charles Khanichi N, Snitow Melinda E, Fazio Sergio, Wiest Michelle M, Watkins Steven M, Linton MacRae F, Hotamisligil Gökhan S, Reducing endoplasmic reticulum stress through a macrophage lipid chaperone alleviates atherosclerosis, 10.1038/nm.2067
  49. Rhee Sue Goo, Woo Hyun Ae, Kil In Sup, Bae Soo Han, Peroxiredoxin Functions as a Peroxidase and a Regulator and Sensor of Local Peroxides, 10.1074/jbc.r111.283432
  50. Murakami Katsuhiro, Ichinohe Yuzuru, Koike Masaaki, Sasaoka Norio, Iemura Shun-ichiro, Natsume Tohru, Kakizuka Akira, VCP Is an Integral Component of a Novel Feedback Mechanism that Controls Intracellular Localization of Catalase and H2O2 Levels, 10.1371/journal.pone.0056012
  51. Wilhelmus Micha M.M., Nijland Philip G., Drukarch Benjamin, de Vries Helga E., van Horssen Jack, Involvement and interplay of Parkin, PINK1, and DJ1 in neurodegenerative and neuroinflammatory disorders, 10.1016/j.freeradbiomed.2012.05.040
  52. Andres-Mateos E., Perier C., Zhang L., Blanchard-Fillion B., Greco T. M., Thomas B., Ko H. S., Sasaki M., Ischiropoulos H., Przedborski S., Dawson T. M., Dawson V. L., DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase, 10.1073/pnas.0703219104
  53. Thomas Kelly Jean, McCoy Melissa K., Blackinton Jeff, Beilina Alexandra, van der Brug Marcel, Sandebring Anna, Miller David, Maric Dragan, Cedazo-Minguez Angel, Cookson Mark R., DJ-1 acts in parallel to the PINK1/parkin pathway to control mitochondrial function and autophagy, 10.1093/hmg/ddq430
  54. Altun Mikael, Edström Erik, Spooner Eric, Flores-Moralez Amilcar, Bergman Esbjörn, Tollet-Egnell Petra, Norstedt Gunnar, Kessler Benedikt M., Ulfhake Brun, Iron load and redox stress in skeletal muscle of aged rats, 10.1002/mus.20808
  55. Budas Grant R., Disatnik Marie-Hélène, Chen Che-Hong, Mochly-Rosen Daria, Activation of aldehyde dehydrogenase 2 (ALDH2) confers cardioprotection in protein kinase C epsilon (PKCɛ) knockout mice, 10.1016/j.yjmcc.2009.10.030
  56. Barski Oleg A., Tipparaju Srinivas M., Bhatnagar Aruni, The Aldo-Keto Reductase Superfamily and its Role in Drug Metabolism and Detoxification, 10.1080/03602530802431439
  57. Kampinga Harm H., Hageman Jurre, Vos Michel J., Kubota Hiroshi, Tanguay Robert M., Bruford Elspeth A., Cheetham Michael E., Chen Bin, Hightower Lawrence E., Guidelines for the nomenclature of the human heat shock proteins, 10.1007/s12192-008-0068-7
  58. Vos Michel J., Hageman Jurre, Carra Serena, Kampinga Harm H., Structural and Functional Diversities between Members of the Human HSPB, HSPH, HSPA, and DNAJ Chaperone Families†, 10.1021/bi800639z
  59. Doran Philip, Gannon Joan, O’Connell Kathleen, Ohlendieck Kay, Aging skeletal muscle shows a drastic increase in the small heat shock proteins αB-crystallin/HspB5 and cvHsp/HspB7, 10.1016/j.ejcb.2007.07.003
  60. Mymrikov E. V., Seit-Nebi A. S., Gusev N. B., Large Potentials of Small Heat Shock Proteins, 10.1152/physrev.00023.2010
  61. Acunzo Julie, Katsogiannou Maria, Rocchi Palma, Small heat shock proteins HSP27 (HspB1), αB-crystallin (HspB5) and HSP22 (HspB8) as regulators of cell death, 10.1016/j.biocel.2012.04.002
  62. Kim Yujin E., Hipp Mark S., Bracher Andreas, Hayer-Hartl Manajit, Ulrich Hartl F., Molecular Chaperone Functions in Protein Folding and Proteostasis, 10.1146/annurev-biochem-060208-092442
  63. Iosefson Ohad, Sharon Shelly, Goloubinoff Pierre, Azem Abdussalam, Reactivation of protein aggregates by mortalin and Tid1—the human mitochondrial Hsp70 chaperone system, 10.1007/s12192-011-0285-3
  64. Taipale Mikko, Jarosz Daniel F., Lindquist Susan, HSP90 at the hub of protein homeostasis: emerging mechanistic insights, 10.1038/nrm2918
  65. Boyan Barbara D., Chen Jiaxuan, Schwartz Zvi, Mechanism of Pdia3-dependent 1α,25-dihydroxy vitamin D3 signaling in musculoskeletal cells, 10.1016/j.steroids.2012.04.018
  66. Chen Jiaxuan, Lobachev Kirill S., Grindel Brian J., Farach-Carson Mary C., Hyzy Sharon L., El-Baradie Khairat B., Olivares-Navarrete Rene, Doroudi Maryam, Boyan Barbara D., Schwartz Zvi, Chaperone Properties of Pdia3 Participate in Rapid Membrane Actions of 1α,25-Dihydroxyvitamin D3, 10.1210/me.2012-1277
  67. Muir Susan W., Montero-Odasso Manuel, Effect of Vitamin D Supplementation on Muscle Strength, Gait and Balance in Older Adults: A Systematic Review and Meta-Analysis, 10.1111/j.1532-5415.2011.03733.x
  68. Bechet Daniel, Tassa Amina, Taillandier Daniel, Combaret Lydie, Attaix Didier, Lysosomal proteolysis in skeletal muscle, 10.1016/j.biocel.2005.02.029
  69. Attaix Didier, Bechet Daniel, FoxO3 Controls Dangerous Proteolytic Liaisons, 10.1016/j.cmet.2007.11.005
  70. Meyer Hemmo, Bug Monika, Bremer Sebastian, Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system, 10.1038/ncb2407
  71. Ye Yihong, Meyer Hemmo H., Rapoport Tom A., The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol, 10.1038/414652a
  72. Xu S., Peng G., Wang Y., Fang S., Karbowski M., The AAA-ATPase p97 is essential for outer mitochondrial membrane protein turnover, 10.1091/mbc.e10-09-0748
  73. Kim Johnny, Löwe Thomas, Hoppe Thorsten, Protein quality control gets muscle into shape, 10.1016/j.tcb.2008.03.007
  74. Ye Yihong, Diverse functions with a common regulator: Ubiquitin takes command of an AAA ATPase, 10.1016/j.jsb.2006.01.005
  75. Krick Roswitha, Bremer Sebastian, Welter Evelyn, Schlotterhose Petra, Muehe Yvonne, Eskelinen Eeva-Liisa, Thumm Michael, Cdc48/p97 and Shp1/p47 regulate autophagosome biogenesis in concert with ubiquitin-like Atg8, 10.1083/jcb.201002075
  76. Tanaka Atsushi, Cleland Megan M., Xu Shan, Narendra Derek P., Suen Der-Fen, Karbowski Mariusz, Youle Richard J., Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin, 10.1083/jcb.201007013
  77. Altun Mikael, Besche Henrike C., Overkleeft Herman S., Piccirillo Rosanna, Edelmann Mariola J., Kessler Benedikt M., Goldberg Alfred L., Ulfhake Brun, Muscle Wasting in Aged, Sarcopenic Rats Is Associated with Enhanced Activity of the Ubiquitin Proteasome Pathway, 10.1074/jbc.m110.129718
  78. Bergink Steven, Toussaint Wendy, Luijsterburg Martijn S., Dinant Christoffel, Alekseev Sergey, Hoeijmakers Jan H.J., Dantuma Nico P., Houtsmuller Adriaan B., Vermeulen Wim, Recognition of DNA damage by XPC coincides with disruption of the XPC–RAD23 complex, 10.1083/jcb.201107050
  79. Wade Staton L., Auble David T., The Rad23 ubiquitin receptor, the proteasome and functional specificity in transcriptional control, 10.4161/trns.1.1.12201
  80. Lei Yu, Wen Haitao, Ting Jenny P.Y., The NLR protein, NLRX1, and its partner, TUFM, reduce type I interferon, and enhance autophagy, 10.4161/auto.23026
  81. Besio Roberta, Baratto Maria Camilla, Gioia Roberta, Monzani Enrico, Nicolis Stefania, Cucca Lucia, Profumo Antonella, Casella Luigi, Basosi Riccardo, Tenni Ruggero, Rossi Antonio, Forlino Antonella, A Mn(II)–Mn(II) center in human prolidase, 10.1016/j.bbapap.2012.09.008
  82. Zhang Huina, Wang Yang, Li Jing, Yu Jinhai, Pu Jing, Li Linghai, Zhang Hongchao, Zhang Shuyan, Peng Gong, Yang Fuquan, Liu Pingsheng, Proteome of Skeletal Muscle Lipid Droplet Reveals Association with Mitochondria and Apolipoprotein A-I, 10.1021/pr200553c
  83. Bearden Shawn E., Effect of Aging on the Structure and Function of Skeletal Muscle Microvascular Networks, 10.1080/10739680600618892
  84. Scott H. S., Chen Haiming, Rossier Colette, Lalioti Maria D., Antonarakis Stylianos E., Isolation of a human gene (HES1) with homology to an Escherichia coli and a zebrafish protein that maps to chromosome 21q22.3, 10.1007/s004390050416
  85. Aksoy Pinar, Zhu Min Jia, Kalari Krishna R., Moon Irene, Pelleymounter Linda L., Eckloff Bruce W., Wieben Eric D., Yee Vivien C., Weinshilboum Richard M., Wang Liewei, Cytosolic 5′-nucleotidase III (NT5C3): gene sequence variation and functional genomics : , 10.1097/fpc.0b013e32832c14b8
  86. Sato Yusuke, Probst Hans Christian, Tatsumi Ryuichi, Ikeuchi Yoshihide, Neuberger Michael S., Rada Cristina, Deficiency in APOBEC2 Leads to a Shift in Muscle Fiber Type, Diminished Body Mass, and Myopathy, 10.1074/jbc.m109.052977
  87. Sayd Thierry, Morzel Martine, Chambon Christophe, Franck Michel, Figwer Philippe, Larzul Catherine, Le Roy Pascale, Monin Gabriel, Chérel Pierre, Laville Elisabeth, Proteome Analysis of the Sarcoplasmic Fraction of PigSemimembranosusMuscle:  Implications on Meat Color Development, 10.1021/jf052569v
  88. Vizcaíno Juan A, Deutsch Eric W, Wang Rui, Csordas Attila, Reisinger Florian, Ríos Daniel, Dianes José A, Sun Zhi, Farrah Terry, Bandeira Nuno, Binz Pierre-Alain, Xenarios Ioannis, Eisenacher Martin, Mayer Gerhard, Gatto Laurent, Campos Alex, Chalkley Robert J, Kraus Hans-Joachim, Albar Juan Pablo, Martinez-Bartolomé Salvador, Apweiler Rolf, Omenn Gilbert S, Martens Lennart, Jones Andrew R, Hermjakob Henning, ProteomeXchange provides globally coordinated proteomics data submission and dissemination, 10.1038/nbt.2839
Bibliographic reference Gueugneau, Marine ; Coudy-Gandilhon, Cécile ; Gourbeyre, Ophélie ; Chambon, Christophe ; Combaret, Lydie ; et. al. Proteomics of muscle chronological ageing in post-menopausal women. In: BMC Genomics, Vol. 15, no.1, p. 1165 [1-25] (2014)
Permanent URL http://hdl.handle.net/2078.1/173412