УЛЬТРАСТРУКТУРНЫЕ ИЗМЕНЕНИЯ ВНУТРИКЛЕТОЧНЫХ ОРГАНЕЛЛ ПРИ АПОПТОЗЕ

Е.С. Снигиревская, Я.Ю. Комиссарчик

Аннотация


Гибель клеток в результате генетически запрограммированных процессов апоптоза принимает участие не только в эмбриогенезе и гистогенезе, но также является фактором патогенеза многих заболеваний, в том числе вызываемых факторами окружающей среды, и может индуцироваться ими. В последнее время на первый план вышли исследования молекулярных механизмов апоптоза. В настоящем обзоре основное внимание уделено современным данным об ультраструктурных особенностях основных клеточных органелл и об их изменениях в процессе апоптоза, в том числе перестройкам компонентов интерхроматинового пространства ядра, а также участию убиквитин-протеасомной системы в апоптозе.

Ключевые слова


апоптоз, внутриклеточные органеллы, ультраструктура, хроматин, электронная микроскопия, убиквитин-протеасомная система.

Полный текст:

PDF

Как процитировать материал

Литература


Блинов ЛН, Перфилова ИЛ, Юмашева ЛВ. Экологическая обстановка и здоровье человека. В кн.: Всероссийский форум «Пироговская хирургическая неделя» к 200-летию Н.И. Пирогова. СПб.; 2010. c. 143-8.

Боголюбов ДС. Перихроматиновый компартмент клеточного ядра. Цитология. 2014;56:399-409.

Зайкова ЮЯ, Евтеева ИН, Цимоха АС. Протеасомы и их возможная роль во внеклеточном пространстве. Цитология, 2013;55:753-60.

Залесский ВН, Великая НВ. Методы ранней диагностики апоптоза in vitro и in vivo для оценки хронических эффектов токсикантов. Совр пробл токсикол. 2006;1:78-82.

Залесский ВН, Гавриленко ТИ. Апоптоз при ишемии и реперфузии миокарда. Врач дело. 2002;(1):815-6.

Збарский ИБ, Кузьмина СВ. Скелетные структуры клеточного ядра. М.: Наука; 1991.

Минуллина РТ, Фахруллин РФ, Ишмухаметова ДГ. Caenorhabditis elegans в токсикологии и нанотоксикологии. Вестник ВГУ, Сер Хим биол фармац. 2012;2:172-82.

Орлова ДД, Трибулович ВГ, Гарабаджиу АВ и др. Роль митохондриального морфогенеза в регуляции апоптоза. Цитология, 2015;57(3):184-91.

Соколова ЮЯ, Снигиревская ЕС, Комиссарчик ЯЮ. Аппарат Гольджи паразитических простейших (Обзор литературы). Цитология, 2007;49(3):163-81.

Снигиревская ЕС, Комиссарчик ЯЮ. Электронно-микроскопическое выявление протеасом в апоптозных клетках U-937. ДАН. 2014;454:733-6.

Снигиревская ЕС, Мошков АВ, Юринская ВЕ и др. Ультраструктурный и рентгеновский микроанализ клеток U937 при апоптозе, индуцированном гипертонией. Cell Tiss Biol, 2015; 9(2):96-109.

Снигиревская ЕС, Соколова ЮЯ, Комиссарчик ЯЮ. Структурно-функциональная организация аппарата Гольджи. Цитология. 2006;48(4):283-307.

Цимоха АС. Протеасомы: участие в клеточных процессах. Цитология. 2010;52(4):277-300.

Чумаков ПМ. Белок р53 и его универсальные функции в многоклеточных организмах. Успехи биологической химии. 2007;47:3-52.

Шашова ЕЕ, Колегова ЕС, Кондакова ИВ, Завьялов АА. Внутриклеточный и циркулирующий пулы протеасом: значение при злокачественных новообразованиях различных локализаций. Сиб онкол журн. 2015;(6):76-82.

Blinov LN, Perfilova IL, Yumasheva LV. [Ecological conditions and human health]. In: Vserossiyskiy Forum “Pirogovskaya Khirurgicheskaya Nedelia” k 200-Letiyu N.I. Pirogova. Saint Petersburg; 2010. p 143-8. (In Russ.)

Bogoliubov DS. [The perichromatin compartment of the cell nucleus]. Tsytologiya 2014;56:399-409. (In Russ.)

Zaykova YuYa, Yevteyeva IN, Tsymokha AS. [Proteasomes and their possible role in the extracellular space]. Tsitologiya, 2013;55:753-60. (In Russ.)

Zalessky VN, Velikaya NV. [Methods of early diagnosis of apoptosis in vitro and in vivo for evaluation of chronic effects of toxicants]. Sovremennye Problemy Toksikologii. 2006;1:78-82. (In Russ.)

Zalessky VN, Gavrilenko TI. [Apoptosis at ischemia and myocardial reperfusion]. Vrachebnoye Delo, 2002(1):815-6. (In Russ.)

Zbarsky IB, Kuzmina SV. Skelentye Struktury Kletochnogo Yadra. [Skeletal Structures of Cell Nucleus]. M.: Nauka; 1991. (In Russ.)

Minullina RT, Fakhrullin RF, Ishmukhametova DG. [Caenorhabditis elegans in toxicology and nanotoxicology]. Vestnik VGU Ser. Khim Biol Pharm. 2012;2:172-82. (In Russ.)

Orlova DD, Tribulovich VG, Garabadzhiu AV et al. [The role of mitochondrial dynamics in regulation of apoptosis]. Tsitologiya. 2015;57(3):184-191. (In Russ.)

Sokolova YuYa, Snigirevskaya YeS, Komissarchik YaYu. [Golgi apparatus in parasitic protozoa: A Review]. Tsitologiya. 2007;49(3):163-81. (In Russ.)

Snigirevskaya YeS, Komissarchik YaYu. [Electron microscopic detection of proteasomes in apoptotic U-937 cells]. Dokl Ross Akad Nauk. 2014;454:733-6. (In Russ.)

Snigirevskaya YeS, Moshkov AV, Yurinskaya VYe et al. [Ultrastructural and X-ray analysis of U937 cells upon hypertension-induced apoptosis]. Cell and Tissue Biology, 2015;9(2):96-109. (In Russ.)

Snigirevskaya YeS, Sokolova YuYa, Komissarchik YaYu. [Structural and functional organization of Golgi apparatus]. Tsitologiya. 2006;48(4):283307. (In Russ.)

Tsimokha AS. [Proteasomes: Their role in cellular processes]. Tsitologiya. 2010;52(4):277-300. (In Russ.)

Chumakov PM. [p53 protein and its versatile functions in multicellular organisms]. Uspekhi Biologicheskoy Khimii, 2007;47:3-52. (In Russ.)

Shashova YeYe, Kollegova YeS, Kondakova IV, Zavyalov AA. [The intracellular and circulating pools of proteasomes: Their significance in neoplasms having different locations]. Sibirskiy Onkologicheskiy Zhurnal. 2015;6:76-82. (In Russ.)

Ahsen von O, Renken C, Perkins G et al. Preservation of mitochondrial structure and function after Bid- or Bax-mediated cytochrome c release. J Cell Biol. 2000;150:1027-36.

Arden N, Betenbaugh MJ. Life and death in mammalian cell culture: strategies for apoptosis inhibition. Trends Biotechnol. 2004;22:174-80.

Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science. 1998;281:1305-8.

Babbit SE, Kiss A, Deffenbaugh AE et al. ATP hydrolysis-dependent disassembly of the 26S proteasome is a part of the catalytic cycle. Cell. 2005;121:663-5.

Baldin V, Militello M, Thomas Y et al. A novel role for PA28g proteasome in nuclear speckle organization and SR protein trafficking. Mol Biol. 2008;19:1706-16.

Basello D, Cisterna B, Galimberti V et al. Ultrastructural cytochemistry as a tool for studying transcriptional mechanisms. In: Pellicciari C, de Bernardi F, de Carli L (eds.). The Genome and Its Expression through the Microscope. The Legacy of Maria Gabriella Manfredi Romanini. 2015; p. 35-44.

Bassik MC, Scorrano L, Oakes SA et al. Phosphorylation of Bcl-2 regulates ER Ca2+homeostasis and apoptosis. EMBO J. 2004;23:1207-16.

Biggiogera M, Bottone MG, Pellicciari C. Nuclear ribonucleoprotein-containing structures undergo severe rearrangement during spontaneous thymocyte apoptosis. A morphological study by electron microscopy. Histochem Cell Biol. 1997;107:331-6.

Biggiogera M, Bottone MG, Scovassi AI et al. Rearrangement of nuclear ribonucleoprotein (RNP)-containing structures during apoptosis and transcriptional arrest. Biol Cell. 2004; 96:603-15.

Biggiogera M, Cisterna B, Bottone MG et al. Nuclear RNP and nucleolar-associated proteins during apoptosis: A politically correct form of segregation? Dyn Cell Biol. 2007;1:65-71.

Biggiogera M, Cisterna B, Spedito A et al. Perichromatin fibrils as early markers of transcriptional alterations. Differentiation 2008;76:57-65.

Biggiogera M, Bottone MG, Pelliciari C. Nuclear RNA is extruded from apoptotic cells. J Histochem Cytochem. 1998;46:999-1005.

Biggiogera M, Fakan S. Fine structural specific visualization of RNA on ultrathin 24,25, sections. J Histochem Cytochem. 1998;46:389-95.

Biggiogera M, Fakan S, Visualization of nuclear organization by ultrastructural cytochemistry. Meth Cell Biol. 2008;88:431-49.

Biggiogera M, Pellicciari C. Heterogeneous ectopic RNP-derived structures (HERDS) are markers of transcriptional arrest. FASEB J. 2000;14:828-34.

Bonnano E, Tagliafierro G, Carla EC et al. Synchronized onset of nuclear and cell surface modifications in U937 cells during apoptosis. Eur J Histochem. 2002;46:61-74.

Borner C. The Bcl-2 protein family: Sensors and checkpoints for life-or-death decisions. Mol Immunol. 2003;39:615-47.

Bottone MG, Santin G, Aredia F et al. Morphological features of organelle during apoptosis: an overview. Cells. 2013;2:294-305.

Boya P, Cohen I, Zamzami N et al. Endoplasmic reticulum stress-induced cell death requires mitochondrial membrane permeabilization. Cell Death Differ. 2002;9:465-67.

Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974;77:71-94.

Ciechanover A, Hod Y, Hershko A. A heat-stable polypeptide component of an ATP-dependent proteolytic system from reticulocytes. Biochem Biophys Res Commun. 1978;81:1100-05.

Chiu R, Novikov L, Mukherjee S, Shields D. A caspase cleavage fragment of p115 induces fragmentation of the Golgi apparatus and apoptosis. J Cell Biol. 2002;159(4):349-57.

Cohen-Kaplan V, Livneh I, Avnil N et al. The ubiquitin-proteasome system and autophagy: Coordinated and independent activities. Int J Biochem Cell Biol. 2016;79:403-18.

Cory S, Huang DC, Adams JM. The Bcl-2 family: Roles in cell survival and oncogenesis. Oncogene 2003;22:8590-607.

Delbridge A, Strasser A. The Bcl-2 protein family, BH3-mimetics and cancer therapy. Cell Death Different. 2015;22:1071-80.

DesouzaM, Gunning PW, Stehn JR. Theactin cytoskeleton as a sensor and mediator of apoptosis. Bioarchitecture. 2012;2:75-87.

Dewson G, Kluck RM. Bcl-2 family-regulated apoptosis in health and disease. Cell Health Cytoskelet. 2010;2;9-22.

Elmore S. Apoptosis: A review of programmed cell death. Toxicol Pathol. 2007;35(4):495516.

Enenkel C. Proteasome dynamics. Biochim Biophys Acta. 2014;1843:39-46.

Enenkel C. Proteasome dynamics: Will the territory of proteasomes be claimed by mitochondrial proteases under stress conditions? Biochem Mol Biol J. 2017;3:2-3.

Ernster L, Schatz G. Mitochondria: A historical review. J Cell Biol. 1981;91:227s-55s.

Fakan S. Perichromatin fibrils are in situ forms of nascent transcripts. Trends Cell Biol.1994;4:86-90.

Fakan S. The functional architecture of the nucleus as analysed by ultrastructural cytochemistry. Histochem Cell Biol. 2004;122:83-93.

Farquhar G, Palade G. The Golgi apparatus (complex): From artifact to center stage. J Cell Biol. 1981;91:77-103.

Fava LL, Bock FJ, Geley S, Villunger A. Caspase-2 at a glance. J Cell Sci. 2012;125:5911-15.

Favaloro B, Allocati N, Graziano V et al. Role of apoptosis in disease, Aging. 2012;4:330-49.

Fernald K, Kurokawa M. Evading apoptosis in cancer. Trends Cell Biol. 2013;23:620-33.

Finley D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem. 2009;78:477-513.

Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW et al. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Develop Cell. 2001;1:515-25.

Frey TG, Renken CW, Perkins GA. Insight into mitochondrial structure and function from electron tomography. Biochim Biophys Acta. 2002;1555:196-203.

Fulda S. Tumor resistance to apoptosis. Int J Cancer. 2009;124:511-5.

Gallo C, Munro E, Rasoloson D et al. Processing bodies and germ granules are distinct RNA granules that interact in C. elegans embryos. Dev Biol. 2008;323:76-87.

Gao X, Li J, Pratt G et al. Purification procedures determine the proteasome activation properties of REGg (PA28g). Arch Biochem Biophys 2004;425:158-64.

Giussani P, Tringali C, Riboni L et al. Sphingolipids: Key regulators of apoptosis and pivotal players in cancer drug resistance. Int J Mol Sci. 2014;15:4356-92.

Goldberg AL. Protein degradation and protection against misfolded or damaged proteins. Nature. 2003;426:895-99.

Groll M, Ditzel L, Lowe J et al. Crystallization and preliminary X-ray analysis of the Thermoplasma acidophilum 20S proteasome in complex with protein substrates. Nature. 1997;386: 463-71.

Groll M, Bochtler M, Brandstetter H et al. Molecular machines for protein degradation. Chem Biochem. 2005;6(2):222-56.

Hakem R, Hakem A, Duncan GS et al. Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell. 1998;94(3):339-52.

Hannani D. Extracorporeal photopheresis: Tolerogenic or immunogenic cell death? Beyond current dogma. Front Immunol. 2015;6:349.

Hannun YA, Obeid LM. Principles of bioactive Lipid signalling: Lessons from sphingolipids. Nat Rev Mol Cell Biol. 2008;9:139-50.

Heath-Engel HM, Shore GC. Regulated targeting of Bax and Bak to intracellular membranes during apoptosis. Cell Death Differ. 2006;13:1277-80.

Hershko A, Ciechanover A, Varshavsky A. Basic medical research award: The ubiquitin system. Nat Med. 2000;6:1073-81.

Hiramatsu N, Chiang W-C, Kurt T et al. Multiple mechanisms of unfolded protein response induced cell death. Am J Pathol. 2015;185:1800e-08e.

Hu R, Ma S, Li H et al. Effect of magnetic fluid hyperthermia on lung cancer nodules in a murine model. Oncol Lett. 2011;2:1161-4.

Huber EM, Basler M, Schwab R et al. Immuno- and constitutive proteasome crystal structures reveal differences in substrate and inhibitor specificity. Cell 2012;148(4):727-38.

Jiang Z, Hu Z, Zeng L, Lu W, Zhang H, Li T, Xiao H. The role of the Golgi apparatus in oxidative Stress: Is this organelle less significant than mitochondria? Free Rad Biol Med. 2011;50:907-17.

Kerr JFR, Wyllie AH, Currie AR. Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26:239-57.

Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, Krammer PH, Peter ME. Cytotoxicity dependent with the receptor. EMBO J 1995;14:5579-88.

Kisselev AF, Garcia-Calvo M, Overkleeft HS et al. The caspase-like sites of proteasomes, their substrate specificity, new inhibitors and substrates, and allosteric interactions with the trypsin-like sites. J Biol Chem. 2003;278(38): 35869-77.

Kloetzel PM, Souza A, Stohwasser R. The role of the proteasome system and the troteasome activator PA28 complex in the cellular immune response. Biol Chem. 1999;380:293-97.

Klumperman J. Transport between ER and Golgi. Curr Opin Cell Biol. 2000;12:445-9.

Klumperman J. Architecture of the mammalian Golgi. Cold Spring Harb Perspect. Biol. 2011;3:a005181.

Korsmeyer SJ. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome C during apoptosis Dev Cell 2002;2:55-67.

Kotaja N, Sassone-Corsi P. The chromatoid body: A germ-cell-specific RNA processing centre. Nat Rev Mol Cell Biol. 2007;8:85-90.

Koyama T, Oike M, Ito Y. Involvement of Rho-kinase and tyrosine kinase in hypotonic stress-induced ATP release in bovine aortic endothelial cells. J Physiol. 2001;532 (3):759-69.

Krammer PH. CD95(APO-1/Fas)-mediated apoptosis: Live and let die. Adv Immunol. 1999;71:163-210.

Lamparska-Przybysz B, Gajkowska B, Motyl T. Cathepsins and Big are involved in the molecular switch between apoptosis and autophagy in breast cancer MCF-7 cells exposed to Campothecin. J Physiol Pharmacol. 2005;56:159-79.

Lane JD, Allan VJ, Woodman PG. Active relocation of chromatin and endoplasmic reticulum into blebs in late apoptotic cells. J Cell Sci. 2005;118:4059-71.

Lapajne J. Detailed Structure of Mitochondrion. Ljubljana; 2015.

Lee YJ, Jeong SY, Karbowski M, Smith CL, Youle RJ. Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol Biol Cell. 2004;15:5001-11.

Leev C. ATP-dependent proteases degrade their substrates unraveling them from the degradation Signal. Mol Cell 2001;7:627-37.

Li H, Zhu H, Xu CJ, Yuan J. Cleavage of Bid by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 1998;94:491-501.

Locksley RM, Killeen N, Lenardo MJ. The TNF and TNF receptor superfamilies: Integrating mammalian biology. Cell 2001;104:487-501.

Lockshin RA, Zakeri Z. Cell death in health and disease. J Cell Mol Med. 2007;11:1214-24.

Lopez J, Tait SWG. Mitochondrial apoptosis: Killing cancer using the enemy within. Brit J Cancer. 2015;112:957-62.

Low P. The role of proteasome in apoptosis. In: Srivastava R (ed.). Apoptosis, Cell Signaling, and Human Diseases: Molecular Mechanisms. Vol2. Totowa, NJ: Humana Press Inc.: 2007.

Lowe M, Lane JD, Woodman PG, Allan VJ. Caspase-mediated cleavage of syntaxin 5 and giantin accompanies inhibition of secretory traffic during apoptosis. J Cell Sci. 2004;117:1139-50.

Lowe J, Stock D, Jap B, Zwickl P, Baumeister W, Huber R. Crystal structure of the 20S proteasome from the Archaeon T. acidophilum at 3.4 A resolution. Science. 1995;268:533-39.

Machamer CE. The Golgi complex in stress and death. Frontiers Neurosci. 2015;9:421-5.

Maghsoudi N, Zakeri Z, Lockshin RA. Programmed cell death and apoptosis–where it came from and where it is going. From Elie Metchnikoff to the control of caspases. Exp Oncol. 2012;34:146-52.

Mala JG, Rose C. Interactions of heat shock protein 47 with collagen and the stress response: An unconventional chaperone model? Life Sci. 2010;87:579-86.

Mancini M, Machamer CE, Roy S, Nicholson DW, Thornberry NA, et al. Caspase-2 is localized at the Golgi complex and cleaves Golgin-160 during apoptosis. J Cell Biol. 2000;149:603-12.

Mannella CA, Pfeiffer DR, Bradshaw PC et al. Topology of the mitochondrial inner membrane: Dynamics and bioenergetic implications. IUBMB Life 2001;52:93-100.

Marceau N, Schutte B, Gilbert S et al. Dual roles of intermediate filaments in apoptosis. Exp Cell Res. 2007;313:2265-81.

Marsden VS, O’Connor L, O’Reilly LA et al. Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome C/Apaf1/ caspase-9 apoptosome. Nature. 2002;419:634-7.

Martinou JC, Green DR. Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol. 2001;2:63-7.

Martinou JC, Youle RJ. Which came first, the cytochrome C release or the mitochondrial fission? Cell Death Differ. 2006;3:1291-95.

Maurer BJ, Metelitsa LS, Seeger RC et al. Increase of ceramide and induction of mixed apoptosis/ necrosis by N-(4-hydroxyphenyl)-retinamide in neuroblastoma cell lines. J Natl Cancer Inst. 2009;91:1138-46.

Meier P, Finch A, Evan G. Apoptosis in development. Nature 2000;407:796-801.

Mironov AA, Beznoussenko GV, Polishchuk RS, Trucco A. Intra-Golgi transport: A way to a new paradigm? Biochim Biophys Acta 2005;1744:340-50.

Mita P, de Luca A, Abbro I, Dini, L. Ultrastructural analysis of apoptosis of U-937 cells conditioned medium. Ital J Zool. 2003;70:141-6.

Mitchell P. Coupling of phosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature. 1961;191:144-8.

Miyata S, Mizuno T, Koyama Y et al. The endoplasmic reticulum-resident chaperone heat shock protein 47 protects the Golgi apparatus from the effects of O-glycosylation inhibition. PloS One. 2013;8:e69732.

Morris EP, da Fonesca PCA. High-resolution cryo-EM proteasome structures in drug development. Acta Cryst. 2017;D73:522-33.

Mosevitsky MI, Snigirevskaya ES., Komissarchik YaYu. Immunoelectronmicroscopic study of BASP1 and MARCKS location in the early and late spermatids. Acta Histochem. 2012;114:237-43.

Moss DK, Lane JD. Microtubules: forgotten players in the apoptotic execution phase. Trends Cell Biol. 2006;16:330-8.

Mueller O, Anlasik T, Wiedeman J et al. Circulating extracellular proteasome in the cerebrospinal fluid: A study on concentration and proteolytic activity. J Mol Neurosci. 2012;46:509-15.

Mukherjee S, Chiu R, Leung SM, Shields D. Fragmentation of the Golgi apparatus: An early apoptotic event independent of the cytoskeleton. Traffic. 2007;8(4):369-78.

Nawrocki ST, Carew JS, Dunner K et al. Bortezomib inhibits PKR-like endoplasmic reticulum (ER) kinase and induces apoptosis via ER stress in human pancreatic cancer cells. Cancer Res 2005;65:11510-9.

Nawrocki ST, Carew JS, Pino MS et al. Bortezomib sensitizes pancreatic cancer cells to endoplasmic reticulum stress-mediated apoptosis. Cancer Res. 2005;65(24):11658-67.

Necchi V, Sommi P, Vanoli A et al. Proteasome particle-rich structures are widely present in human epithelial neoplasm: Correlative light, confocal and electron microscopy study. PLoS One 2011;6:e21.

Neutra M, Leblond CP. Synthesis of the carbohydrate of mucus in the Golgi complex as shown be electron microscope radioautography of goblet cells from rats injected with glucose-H3. J Cell Biol. 1966;30:137-50.

Nyquist K, Martin A. Marching to the beat of the ring: Polypeptide translocation by AAA+ proteases. Trends Biochem Sci. 2014;39:53-60.

Oda E, Ohki R, Murasawa H et al. A BH3-only member of the Bcl-2 family C and candidate mediator of p53-induced apoptosis. Science. 2000;12:1053-8.

Oropeso-Avila M, Vega AF, Maraver JG et al. Emerging roles of apoptotic microtubules during the execution phase of apoptosis. Cytoskeleton, 2015;72:435-46.

Palade G. The fine Structure of mitochondria. Anat Record. 1952;114:427-51.

Palade G. An electron microscope study of the mitochondrial structure. J Histochem Cytochem. 1953;1:188-211.

Palade GE. Intercellular aspects of the process of protein synthesis. Science. 1975;189:347-54.

Paumet F, Brugger B, Parlati F et al. A t-SNARE of the endocytic pathway must be activated for fusion. J Cell Biol. 2001;155:961-68.

Pavlov EV, Priault M, Pietkiewicz D et al. A novel, high conductance channel of nitochondria linked to apoptosisin mammalian cells and Bax expression in yeast. J Cell Biol. 2001;155:725-31.

Pavon D, Cordoba MA, Cotan D et al. Emerging roles of apoptotic microtubules during the execution phase of apoptosis. Cytoskeleton, 2015;72:435-46.

Pelham HR, Rothman JE. The debate about transport in the Golgi: Two sides of the same coin? Cell. 2000;74:71-82.

Pellicciari C, Bottone MG, Scovassi AL et al. Rearrangement of nuclear ribinucleoproteins and extrusion of nucleolus-like bodies during apoptosis induced by hypertonic stress. Eur J Histochem. 2000;44:247-54.

Petrosyan A. Onco-Golgi: Is fragmentation a gate to cancer progression? Biochem Mol Biol J. 2015;1:6-11.

Pickart CM. Back to the future with ubiquitin. Cell 2004;116:181-90.

Pinkel D, Dyer MJ, Martinez-Climent JA. Characterization of 8p21.3 chromosomal deletions in B cell. Blood 2005;106:3214-22.

Rajamahanty S, Alonzo C, Aynehchi S et al. Growth inhibition of androgen-responsive prostate cancer cells with Brefeldin A targeting cell cycle and androgen receptor. J Biomed Sci. 2010;17:5.

Rasheva VI, Domingos PM. Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis. 2009;4:996-1007.

Rastogi PR, Sinha RP. Apoptosis: Molecular mechanisms and pathogenicity. EXCLI J. 2009; 8:155-181.

Rathmell JC, Thompson CB. The central effectors of cell death in the immune system. Annu Rev Immunol. 1999;17:781-828.

Reece SE, Pollitt LC, Colegrave N, Gardner A. The meaning of death: Evolution and ecology of apoptosis inprotozoanparasites. PLoS Pathogens. 2011;7(12):e1002320.

Reyes-Turcu FE, Ventii KH, Wilkinson KD. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem. 2009;78:363-97.

Richardson PG, Barlogie B, Berenson J et al. A Phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med. 2003;348:2609-17.

Rockel TD, Stuhlmann D, Von Mikesz A. Proteasomes degrade proteins in focal subdomains of the human cell nucleus. J Cell Sci. 2005;118:5231-42.

Ryland LK, Fox TE, Liu X et al. Dysregulation of sphingolipid metabolism in cancer. Cancer Biol Ther. 2011;11:138-49.

Rysavy NM, Shimoda LMN, Dixon AM et al. Beyond apoptosis: The mechanism and function of phosphatidyl serine asymmetry in the membrane of activated mast cells. BioArchitecture. 2014;4:45.

Saas P, Kaminski S, Perruche S. Prospects of apoptotic cell based therapies for transplantation and inflammatory diseases. Immunotherapy. 2013; 5:1055-73.

Saraste A, Pulkki K. Morphological and biochemical hallmarks of apoptosis. Cardiovasc Res. 2000;45:528-37.

Savulescu AF, Glickman MH. Proteasome activator 200: the heat is on. Mol Cell Proteomics. 2011;10:1-8.

Schmitz I, Kirchhoff S, Krammer PH. Regulation of death receptor-mediated apoptosis pathways. Int J Biochem Cell Biol. 2000;32:1123-36.

Schreiber A, Peter M. Substrate recognition in selective autophagy and the ubiquitin-proteasome system. Biochem Biophys Acta. 2014;1843:163-81.

Scorrano L, Ashiya M, Buttle K et al. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome C during apoptosis, Dev Cell. 2002;2:55-67.

Scovassi AI, Torriglia A. Activation of DNA-degrading enzymes during apoptosis. Eur J Histochem. 2003;47:185-94.

Shalini S, Dorstyn L, Dawar S, Kumar S. Old, new and emerging functions of caspases. Cell Death Differ. 2015;22:526-39.

Sheridan C, Delivani P, Cullen SP, Martin SJ. Bax or Bak-induced mitochondrial fission can be uncoupled from cytochrome C release. Mol Cell. 2008;31:570-85.

Shiraishi H, Okamoto H, Yoshimura A, Yoshida H. ER stress-induced apoptosis and caspase-12 activation occurs downstream of mitochondrial apoptosis involving Apaf-1. J Cell Sci. 2006;119:3958-66.

Sixt SU, Peters J. Extracellular alveolar proteasomes: Possible role in lung injury and repair. Proc Am Thorac Soc. 2010;7:91-6.

Sjostrand FS. The ultrastructure of cells as revealed by the electron microscope. Int Rev Cytol. 1956;5:455-533.

Snigirevskaya ES, Komissarchik YaYu. Ultrastructural analysis of human leukemia U-937 cells after apoptosis induction: Localization of proteasomes and perichromatin fibers. Acta Histochem, 2017;119:471-80.

Snigirevskaya ES, Mosevitsky MI, Komissarchik YaYu. The role of chromatoid bodies and cytoskeleton in differentiation of rat spermatozoids. Cell Tissue Biol. 2012;6(3):254-67.

Snigirevskaya ES, Moshkov AV, Komissarchik YaYu. Ultrastructural study and X-ray microanalysis of apoptotic lymphoma cells U-937. Biochem Mol Biol J. 2017;3(3):1-2.

Snigirevskaya ES, Moshkov AV, Yurinskaya VE et al. Ultrastructural and X-ray analysis of U937 cells in hypertension induced apoptosis. Cell Tissue Biol. 2015;9(2):96-109.

Solcia P, Sommi P, Necchi V et al. Particle-rich cytoplasmic structure (PaCS): Identification, natural history, role in cell biology and pathology. Biomolecules 2014;4:848-61.

Sommi P, Necchi V, Vitali A et al. PaCS is a novel cytoplasmic structure containing functional proteasome and inducible by cytokines/trophic factors. PLoS One 2013;8:e82560.

Szegezdi E, MacDonald DC, Ni CT, Gupta S, Samali A. Bcl-2 family on guard at the ER. Am J Physiol Cell Physiol. 2009;296:C941-53.

Suess MJ, Huismaus JW (Eds.) Management of Hazardous Waste. Copenhagen: WHO Regional Publication. European Series; 1993.

Sun JY, Yang H, Miao S, Li JP, Wang SW et al. Suppressive effects of swainsonine on C6 glioma cell in vitro and in vivo. Phytomedicine. 2009;16:1070-4.

Sun JY, Zhu MZ, Wang SW, Miao S, Xie YH et al. Inhibition of the growth of human gastric carcinoma in vivo and in vitro by swainsonine. Phytomedicine. 2007;14:353-9.

Tomko RJ, Jr, Hochstrasser M. Molecular architecture and assembly of the eucaryotic proteasome. Annu Rev Biochem. 2013;82:415-45.

Tu J-B, Ma R-Z, Dong Q, Jiang F, Hu X-Y et al. Induction of Apoptosis in Infantile Hemangioma Endothelial Cells by Propranolol. Exp Ther Med 2013; 6: 574-8

Urra H, Dufey E, Lisbona F, Rojas-Rivera D, Hetz C. When ER Stress reaches a dead end. Biochim Biophys Acta 2013;1833:3507-17.

Van der Pol E, Boing AN, Harrison P et al. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol. 2012;64:676-705.

Vasileva A, Tiedau D, Firooznia AM et al. Tdrd6 is required for spermiogenesis, chromatoid body architecture, and regulation of miRNA expression, Curr Biol. 2009;19:630-9.

Voges D, Zwickl P, Baumeister W. The 26S proteasome: A molecular machine designed for controlled proteolysis. Ann Rev Biochem 1999;68:1015-68.

WangY, Seemann J. Golgi biogenesis. Cold Spring Harb Perspect Biol. 2011;3:a005330.

Witkos TM, Lowe M. Recognition and tethering of transport vesicles at the Golgi apparatus. Curr Opin Cell Biol. 2017:47:16-23.

Wojcik C, DeMartino GN. Intracellular localization of proteasomes. Int J Biochem Cell Biol. 2003;35:579-89.

Yamaguchi R, Perkins G. Dynamics of mitochondrial structure during apoptosis and the enigma of Opa. Biochim Biophys Acta.2009;1787(8):963-72.

Yang YL, Li CCH, Weissman AM. Regulating the p53 system through ubiquitination. Oncogene. 2004;23:2096-106.

Zick M, Rabl R, Reichert AS. Cristae formation– linking ultrastructure and function of mitochondria. Biochim Biophys Acta 2009;1793:5-19.

Zoeger A, Blau M, Egerer K, Feist E, Dahlmann B. Circulating proteasomes are functional and have a subtype pattern distinct from 20S proteasomes in major blood cells. Clin Chem. 2006;52:2079-86.




DOI: http://dx.doi.org/10.24855/biosfera.v10i2.440

© ФОНД НАУЧНЫХ ИССЛЕДОВАНИЙ "XXI ВЕК"