Research Progress on Autophagy Regulation by Active Ingredients of Traditional Chinese Medicine in the Treatment of Acute Lung Injury

Abstract Autophagy is a highly conserved process that maintains cell stability in eukaryotes, participates in the turnover of intracellular substances to maintain cell function, helps to resist pathogen invasion, and improves cell tolerance to environmental changes. Autophagy has been observed in many diseases, and the symptoms of these diseases are significantly improved by regulating autophagy. Autophagy is also involved in the development of lung diseases. Studies have shown that autophagy may play a beneficial or harmful role in acute lung injury (ALI), and ALI has been treated with traditional Chinese medicine designed to promote or inhibit autophagy. In this paper, the molecular mechanism and common pathways regulating autophagy and the relationship between autophagy and ALI are introduced, and the active ingredients of traditional Chinese medicine that improve ALI symptoms by regulating autophagy are summarized.

[1]  Z. Zeng,et al.  Cinobufagin alleviates lipopolysaccharide-induced acute lung injury by regulating autophagy through activation of the p53/mTOR pathway , 2022, Frontiers in Pharmacology.

[2]  S. Fakhri,et al.  Polydatin: Pharmacological Mechanisms, Therapeutic Targets, Biological Activities, and Health Benefits , 2022, Molecules.

[3]  Nan Xu,et al.  Sophoridine inhibits endotoxin‐induced acute lung injury by enhancing autophagy of macrophage and reducing inflammation , 2022, Journal of leukocyte biology.

[4]  A. Momtazi-Borojeni,et al.  Berberine as a natural modulator of inflammatory signaling pathways in the immune system: Focus on NF‐κB, JAK/STAT, and MAPK signaling pathways , 2022, Phytotherapy research : PTR.

[5]  Jianhua Fu,et al.  The Role of Autophagy in Lamellar Body Formation and Surfactant Production in Type 2 Alveolar Epithelial Cells , 2022, International journal of biological sciences.

[6]  Fei Luan,et al.  JFNE-A isolated from Jing-Fang n-butanol extract attenuates lipopolysaccharide-induced acute lung injury by inhibiting oxidative stress and the NF-κB signaling pathway via promotion of autophagy. , 2021, Phytomedicine : international journal of phytotherapy and phytopharmacology.

[7]  Zuojia Liu,et al.  AMPK-Mediated Metabolic Switching Is High Effective for Phytochemical Levo-Tetrahydropalmatine (l-THP) to Reduce Hepatocellular Carcinoma Tumor Growth , 2021, Metabolites.

[8]  Jiankui Du,et al.  Resveratrol alleviates acute lung injury through regulating PLSCR-3-mediated mitochondrial dysfunction and mitophagy in a cecal ligation and puncture model. , 2021, European journal of pharmacology.

[9]  Changzheng Zhou,et al.  Sophoridine: A review of its pharmacology, pharmacokinetics and toxicity. , 2021, Phytomedicine : international journal of phytotherapy and phytopharmacology.

[10]  L. Collinson,et al.  Autophagy modulates endothelial junctions to restrain neutrophil diapedesis during inflammation , 2021, Immunity.

[11]  Xuanheng Li,et al.  Circulating mitochondrial DNA-triggered autophagy dysfunction via STING underlies sepsis-related acute lung injury , 2021, Cell Death & Disease.

[12]  Jin Zhang,et al.  Hydrogen-rich saline regulates the polarization and apoptosis of alveolar macrophages and attenuates lung injury via suppression of autophagy in septic rats , 2021, Annals of translational medicine.

[13]  Yong-Qing Zhang,et al.  Toad venom: A comprehensive review of chemical constituents, anticancer activities, and mechanisms , 2021, Archiv der Pharmazie.

[14]  P. Agostinis,et al.  Endothelial cell autophagy in homeostasis and cancer , 2021, FEBS letters.

[15]  L. Braga,et al.  The History and Mystery of Alveolar Epithelial Type II Cells: Focus on Their Physiologic and Pathologic Role in Lung , 2021, International journal of molecular sciences.

[16]  Jia-li Xu,et al.  Oxymatrine exerts a protective effect in myocardial ischemia/reperfusion‑induced acute lung injury by inhibiting autophagy in diabetic rats. , 2021, Molecular medicine reports.

[17]  Dingyu Tan,et al.  Oxyberberine Prevented Lipopolysaccharide-Induced Acute Lung Injury through Inhibition of Mitophagy , 2021, Oxidative medicine and cellular longevity.

[18]  Ningl Wang,et al.  Bone marrow-derived mesenchymal stem cells modulate autophagy in RAW264.7 macrophages via the phosphoinositide 3-kinase/protein kinase B/heme oxygenase-1 signaling pathway under oxygen-glucose deprivation/restoration conditions , 2021, Chinese medical journal.

[19]  Xiujing Feng,et al.  Autophagy Plays a Protective Role in Sodium Hydrosulfide-Induced Acute Lung Injury by Attenuating Oxidative Stress and Inflammation in Rats. , 2021, Chemical research in toxicology.

[20]  Hongli Zhou,et al.  Anti-type I allergic effects of Jing-Fang powder extracts via PI3K/Akt pathway in vitro and in vivo. , 2021, Molecular immunology.

[21]  F. Zhang,et al.  Natural product derived phytochemicals in managing acute lung injury by multiple mechanisms , 2020, Pharmacological Research.

[22]  Weina Wang,et al.  Tetrahydropalmatine protects against acute lung injury induced by limb ischemia/reperfusion through restoring PI3K/AKT/mTOR-mediated autophagy in rats. , 2020, Pulmonary pharmacology & therapeutics.

[23]  J. Kou,et al.  Thalictrum minus L. ameliorates particulate matter-induced acute lung injury in mice. , 2020, Journal of ethnopharmacology.

[24]  Azhar Rasul,et al.  Hispolon: A natural polyphenol and emerging cancer killer by multiple cellular signaling pathways , 2020, Environmental Research.

[25]  Guan-Jhong Huang,et al.  Attenuation of Lipopolysaccharide-Induced Acute Lung Injury by Hispolon in Mice, Through Regulating the TLR4/PI3K/Akt/mTOR and Keap1/Nrf2/HO-1 Pathways, and Suppressing Oxidative Stress-Mediated ER Stress-Induced Apoptosis and Autophagy , 2020, Nutrients.

[26]  Zhanfei Li,et al.  FK866 attenuates sepsis-induced acute lung injury through c-jun-N-terminal kinase (JNK)-dependent autophagy. , 2020, Life sciences.

[27]  Ting Gong,et al.  Bcl-2 Proteins Regulate Mitophagy in Lipopolysaccharide-Induced Acute Lung Injury via PINK1/Parkin Signaling Pathway , 2020, Oxidative medicine and cellular longevity.

[28]  Pingting Zhou,et al.  Metformin induces cell cycle arrest, apoptosis and autophagy through ROS/JNK signaling pathway in human osteosarcoma , 2020, International journal of biological sciences.

[29]  M. Luo,et al.  Cystic fibrosis transmembrane conductance regulator ameliorates lipopolysaccharide-induced acute lung injury by inhibiting autophagy through PI3K/AKT/mTOR pathway in mice , 2019, Respiratory Physiology & Neurobiology.

[30]  J. Kou,et al.  The protective effects of Thalictrum minus L. on lipopolysaccharide-induced acute lung injury. , 2020, Journal of ethnopharmacology.

[31]  T. Beccari,et al.  Hydroxytyrosol: a natural compound with promising pharmacological activities. , 2019, Journal of biotechnology.

[32]  Xiaoting Yang,et al.  Sinomenine attenuates septic‐associated lung injury through the Nrf2‐Keap1 and autophagy , 2019, The Journal of pharmacy and pharmacology.

[33]  Yue Liu,et al.  Oxymatrine Exerts Organ- and Tissue-Protective Effects by Regulating Inflammation, Oxidative Stress, Apoptosis, and Fibrosis: From Bench to Bedside. , 2019, Pharmacological research.

[34]  K. Kuča,et al.  JNK signaling in cancer cell survival , 2019, Medicinal research reviews.

[35]  Huang Zhao,et al.  Astragaloside IV Attenuates Lipopolysaccharides-Induced Pulmonary Epithelial Cell Injury through Inhibiting Autophagy , 2019, Pharmacology.

[36]  L. Tang,et al.  Emodin reactivated autophagy and alleviated inflammatory lung injury in mice with lethal endotoxemia , 2019, Experimental animals.

[37]  Jie Luo,et al.  Inhibitory Effect of Jing-Fang Powder n-Butanol Extract and Its Isolated Fraction D on Lipopolysaccharide-Induced Inflammation in RAW264.7 Cells , 2019, The Journal of Pharmacology and Experimental Therapeutics.

[38]  Jinghua Zhang,et al.  Hydrogen-rich saline ameliorated LPS-induced acute lung injury via autophagy inhibition through the ROS/AMPK/mTOR pathway in mice , 2019, Experimental biology and medicine.

[39]  Xiaoping Yang,et al.  Glycyrrhizic acid ameliorates LPS-induced acute lung injury by regulating autophagy through the PI3K/AKT/mTOR pathway. , 2019, American journal of translational research.

[40]  A. Atanasov,et al.  Resveratrol and Its Effects on the Vascular System , 2019, International journal of molecular sciences.

[41]  A. Randolph,et al.  The acute respiratory distress syndrome. , 1996, New England Journal of Medicine.

[42]  P. Kochanek,et al.  Cardiolipin-Dependent Mitophagy Guides Outcome after Traumatic Brain Injury , 2019, The Journal of Neuroscience.

[43]  Tao Li,et al.  Polydatin mediates Parkin-dependent mitophagy and protects against mitochondria-dependent apoptosis in acute respiratory distress syndrome , 2019, Laboratory Investigation.

[44]  M. Matthay,et al.  Pathogenesis of Acute Respiratory Distress Syndrome , 2019, Seminars in Respiratory and Critical Care Medicine.

[45]  B. Cao,et al.  Rapamycin ameliorates lipopolysaccharide-induced acute lung injury by inhibiting IL-1β and IL-18 production. , 2019, International immunopharmacology.

[46]  Jianhui Xie,et al.  Comparison of anti-inflammatory effects of berberine, and its natural oxidative and reduced derivatives from Rhizoma Coptidis in vitro and in vivo. , 2019, Phytomedicine : international journal of phytotherapy and phytopharmacology.

[47]  Mingshi Yang,et al.  Lipoxin A4 receptor agonist BML-111 induces autophagy in alveolar macrophages and protects from acute lung injury by activating MAPK signaling , 2018, RESPIRATORY RESEARCH.

[48]  Hao Li,et al.  Hydrogen sulfide ameliorated lipopolysaccharide-induced acute lung injury by inhibiting autophagy through PI3K/Akt/mTOR pathway in mice. , 2018, Biochemical and biophysical research communications.

[49]  J. Kou,et al.  YiQiFuMai lyophilized injection attenuates particulate matter-induced acute lung injury in mice via TLR4-mTOR-autophagy pathway. , 2018, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[50]  Zhizhou Yang,et al.  Protective effect of ginsenoside Rg1 on LPS-induced apoptosis of lung epithelial cells. , 2018, Molecular immunology.

[51]  Guan-Jhong Huang,et al.  Ginsenoside Rh2 Ameliorates Lipopolysaccharide-Induced Acute Lung Injury by Regulating the TLR4/PI3K/Akt/mTOR, Raf-1/MEK/ERK, and Keap1/Nrf2/HO-1 Signaling Pathways in Mice , 2018, Nutrients.

[52]  Xiaoliu Zhou,et al.  Ginsenoside Rg3 Attenuates Lipopolysaccharide-Induced Acute Lung Injury via MerTK-Dependent Activation of the PI3K/AKT/mTOR Pathway , 2018, Front. Pharmacol..

[53]  Guangyu Wu,et al.  RAB26-dependent autophagy protects adherens junctional integrity in acute lung injury , 2018, Autophagy.

[54]  G. van den Bogaart,et al.  Endosomal and Phagosomal SNAREs. , 2018, Physiological reviews.

[55]  Fang Han,et al.  Inhibition of autophagy enhanced cobalt chloride-induced apoptosis in rat alveolar type II epithelial cells , 2018, Molecular medicine reports.

[56]  Dong Wang,et al.  ERK1/2/mTOR/Stat3 pathway-mediated autophagy alleviates traumatic brain injury-induced acute lung injury. , 2018, Biochimica et biophysica acta. Molecular basis of disease.

[57]  Ni Wang,et al.  The Role of Autophagy and the Chemokine (C-X-C Motif) Ligand 16 During Acute Lung Injury in Mice , 2018, Medical science monitor : international medical journal of experimental and clinical research.

[58]  S. Slavin,et al.  Autophagy inhibitor 3-methyladenine protects against endothelial cell barrier dysfunction in acute lung injury. , 2018, American journal of physiology. Lung cellular and molecular physiology.

[59]  S. Akira,et al.  Autophagy limits activation of the inflammasomes , 2018, Immunological reviews.

[60]  G. Wells,et al.  Reversible Keap1 inhibitors are preferential pharmacological tools to modulate cellular mitophagy , 2017, Scientific Reports.

[61]  Takafumi Suzuki,et al.  Stress-sensing mechanisms and the physiological roles of the Keap1–Nrf2 system during cellular stress , 2017, The Journal of Biological Chemistry.

[62]  C. Mancuso,et al.  Panax ginseng and Panax quinquefolius: From pharmacology to toxicology , 2017, Food and Chemical Toxicology.

[63]  Lorenzo Galluzzi,et al.  Pharmacological modulation of autophagy: therapeutic potential and persisting obstacles , 2017, Nature Reviews Drug Discovery.

[64]  Y. He,et al.  Hydroxytyrosol Attenuates LPS-Induced Acute Lung Injury in Mice by Regulating Autophagy and Sirtuin Expression. , 2017, Current molecular medicine.

[65]  K. Cadwell.  Crosstalk between autophagy and inflammatory signalling pathways: balancing defence and homeostasis , 2016, Nature Reviews Immunology.

[66]  J. Backer.  The intricate regulation and complex functions of the Class III phosphoinositide 3-kinase Vps34. , 2016, The Biochemical journal.

[67]  Emma Gordon,et al.  Mechanisms and regulation of endothelial VEGF receptor signalling , 2016, Nature Reviews Molecular Cell Biology.

[68]  S. Akira,et al.  Regulation of inflammasomes by autophagy. , 2016, The Journal of allergy and clinical immunology.

[69]  J. Kou,et al.  Simultaneous Qualitative and Quantitative Analysis of Multiple Chemical Constituents in YiQiFuMai Injection by Ultra-Fast Liquid Chromatography Coupled with Ion Trap Time-of-Flight Mass Spectrometry , 2016, Molecules.

[70]  M. Balaan,et al.  Acute Respiratory Distress Syndrome , 2016, Critical care nursing quarterly.

[71]  S. Mok,et al.  New Potential Pharmacological Functions of Chinese Herbal Medicines via Regulation of Autophagy , 2016, Molecules.

[72]  N. Mizushima,et al.  Autophagy machinery in the context of mammalian mitophagy. , 2015, Biochimica et biophysica acta.

[73]  Jun She,et al.  Bone marrow-derived mesenchymal stem cells enhance autophagy via PI3K/AKT signalling to reduce the severity of ischaemia/reperfusion-induced lung injury , 2015, Journal of cellular and molecular medicine.

[74]  C. Germer,et al.  Soluble VE-cadherin is involved in endothelial barrier breakdown in systemic inflammation and sepsis. , 2015, Cardiovascular research.

[75]  D. Green,et al.  Molecular characterization of LC3-associated phagocytosis reveals distinct roles for Rubicon, NOX2 and autophagy proteins , 2015, Nature Cell Biology.

[76]  Y. Li,et al.  MAPK/JNK signalling: a potential autophagy regulation pathway , 2015, Bioscience reports.

[77]  D Andrews,et al.  Essential versus accessory aspects of cell death: recommendations of the NCCD 2015 , 2014, Cell Death and Differentiation.

[78]  Jiqi Yan,et al.  Complement C5a exacerbates acute lung injury induced through autophagy-mediated alveolar macrophage apoptosis , 2014, Cell Death and Disease.

[79]  T. Finkel,et al.  Cellular mechanisms and physiological consequences of redox-dependent signalling , 2014, Nature Reviews Molecular Cell Biology.

[80]  R. Youle,et al.  Self and nonself: how autophagy targets mitochondria and bacteria. , 2014, Cell host & microbe.

[81]  D. Klionsky,et al.  An overview of autophagy: morphology, mechanism, and regulation. , 2014, Antioxidants & redox signaling.

[82]  Eric H. Baehrecke,et al.  Self-consumption: the interplay of autophagy and apoptosis , 2014, Nature Reviews Molecular Cell Biology.

[83]  D. Green,et al.  Anthracyclines induce DNA damage response-mediated protection against severe sepsis. , 2013, Immunity.

[84]  Simon C Watkins,et al.  Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells , 2013, Nature Cell Biology.

[85]  P. Kubes,et al.  Neutrophil recruitment and function in health and inflammation , 2013, Nature Reviews Immunology.

[86]  J. Dubuisson,et al.  Inflammasome Components Coordinate Autophagy and Pyroptosis as Macrophage Responses to Infection , 2013, mBio.

[87]  S. Ryter,et al.  Autophagy in human health and disease. , 2013, The New England journal of medicine.

[88]  D. Rubinsztein,et al.  Autophagy modulation as a potential therapeutic target for diverse diseases , 2012, Nature Reviews Drug Discovery.

[89]  S. Wilkinson,et al.  Src‐dependent autophagic degradation of Ret in FAK‐signalling‐defective cancer cells , 2012, EMBO reports.

[90]  Joseph A. Hill,et al.  Impaired Autophagosome Clearance Contributes to Cardiomyocyte Death in Ischemia/Reperfusion Injury , 2012, Circulation.

[91]  Arthur S Slutsky,et al.  Acute Respiratory Distress Syndrome The Berlin Definition , 2012 .

[92]  D. Gozuacik,et al.  Cleavage of Atg3 protein by caspase-8 regulates autophagy during receptor-activated cell death , 2012, Apoptosis.

[93]  L. Collinson,et al.  Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy , 2012, Molecular biology of the cell.

[94]  S. Amin,et al.  Autophagosomal Membrane Serves as Platform for Intracellular Death-inducing Signaling Complex (iDISC)-mediated Caspase-8 Activation and Apoptosis* , 2012, The Journal of Biological Chemistry.

[95]  Insil Kim,et al.  Mitophagy selectively degrades individual damaged mitochondria after photoirradiation. , 2011, Antioxidants & redox signaling.

[96]  M. Matthay,et al.  The acute respiratory distress syndrome: pathogenesis and treatment. , 2011, Annual review of pathology.

[97]  H. Virgin,et al.  Autophagy in immunity and inflammation , 2011, Nature.

[98]  S. Ryter,et al.  Autophagy proteins regulate innate immune response by inhibiting NALP3 inflammasome-mediated mitochondrial DNA release , 2010, Nature Immunology.

[99]  W. Hou,et al.  Autophagic degradation of active caspase-8 , 2010, Autophagy.

[100]  Ana Maria Cuervo,et al.  Chaperone-mediated autophagy: molecular mechanisms and physiological relevance. , 2010, Seminars in cell & developmental biology.

[101]  A. Lapucci,et al.  Inhibition of Nicotinamide Phosphoribosyltransferase , 2010, Journal of Biological Chemistry.

[102]  M. McMahon,et al.  p62/SQSTM1 Is a Target Gene for Transcription Factor NRF2 and Creates a Positive Feedback Loop by Inducing Antioxidant Response Element-driven Gene Transcription* , 2010, The Journal of Biological Chemistry.

[103]  Sandra Barth,et al.  Autophagy: cellular and molecular mechanisms , 2010, The Journal of pathology.

[104]  Daniel J Klionsky,et al.  Mammalian autophagy: core molecular machinery and signaling regulation. , 2010, Current opinion in cell biology.

[105]  N. Mizushima,et al.  Methods in Mammalian Autophagy Research , 2010, Cell.

[106]  D. Rubinsztein,et al.  Apoptosis blocks Beclin 1-dependent autophagosome synthesis – an effect rescued by Bcl-xL , 2009, Cell Death and Differentiation.

[107]  G. Downey,et al.  Transepithelial migration of neutrophils: mechanisms and implications for acute lung injury. , 2009, American journal of respiratory cell and molecular biology.

[108]  J. Guan,et al.  Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. , 2009, Molecular biology of the cell.

[109]  C. Jung,et al.  ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. , 2009, Molecular biology of the cell.

[110]  S. Akira,et al.  Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages , 2009, Nature Cell Biology.

[111]  D. Klionsky,et al.  An overview of the molecular mechanism of autophagy. , 2009, Current topics in microbiology and immunology.

[112]  R. Youle,et al.  Parkin is recruited selectively to impaired mitochondria and promotes their autophagy , 2008, The Journal of cell biology.

[113]  Daniel J Klionsky,et al.  The Atg8 and Atg12 ubiquitin‐like conjugation systems in macroautophagy , 2008, EMBO reports.

[114]  F. Orsenigo,et al.  Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5 , 2008, Nature Cell Biology.

[115]  S. Pattingre,et al.  JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. , 2008, Molecular cell.

[116]  J. Ting,et al.  Akt-dependent regulation of NF-{kappa}B is controlled by mTOR and Raptor in association with IKK. , 2008, Genes & development.

[117]  B. Levine,et al.  p53: The Janus of autophagy? , 2008, Nature Cell Biology.

[118]  B. Turk,et al.  AMPK phosphorylation of raptor mediates a metabolic checkpoint. , 2008, Molecular cell.

[119]  Z. Malam,et al.  Pre‐B cell colony‐enhancing factor (PBEF)/visfatin: a novel mediator of innate immunity , 2008, Journal of leukocyte biology.

[120]  J. Backer.  The regulation and function of Class III PI3Ks: novel roles for Vps34. , 2008, The Biochemical journal.

[121]  J. J. Mul,et al.  Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis , 2007, Nature Cell Biology.

[122]  Guido Kroemer,et al.  Self-eating and self-killing: crosstalk between autophagy and apoptosis , 2007, Nature Reviews Molecular Cell Biology.

[123]  D. Rubinsztein,et al.  Potential therapeutic applications of autophagy , 2007, Nature Reviews Drug Discovery.

[124]  E. Eskelinen.  Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy. , 2006, Molecular aspects of medicine.

[125]  Takahiro Shibata,et al.  Oxidative and Electrophilic Stresses Activate Nrf2 through Inhibition of Ubiquitination Activity of Keap1 , 2006, Molecular and Cellular Biology.

[126]  Michael D. Schneider,et al.  Bcl-2 Antiapoptotic Proteins Inhibit Beclin 1-Dependent Autophagy , 2005, Cell.

[127]  Paul Tempst,et al.  Phosphorylation and Functional Inactivation of TSC2 by Erk Implications for Tuberous Sclerosisand Cancer Pathogenesis , 2005, Cell.

[128]  Daniel J. Klionsky,et al.  Autophagy in Health and Disease: A Double-Edged Sword , 2004, Science.

[129]  M. Colombo,et al.  Rab7 is required for the normal progression of the autophagic pathway in mammalian cells , 2004, Journal of Cell Science.

[130]  K. Inoki,et al.  TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling , 2002, Nature Cell Biology.

[131]  J. Pugin,et al.  Cytokine balance in the lungs of patients with acute respiratory distress syndrome. , 2001, American journal of respiratory and critical care medicine.

[132]  Y. Ohsumi,et al.  Ubiquitin and proteasomes: Molecular dissection of autophagy: two ubiquitin-like systems , 2001, Nature Reviews Molecular Cell Biology.

[133]  C. Haslett,et al.  Cellular mechanisms of acute lung injury: implications for future treatment in the adult respiratory distress syndrome. , 1992, Thorax.

[134]  E. Cadenas,et al.  Oxidative stress: damage to intact cells and organs. , 1985, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[135]  H. Glaumann,et al.  Autophagy, heterophagy, microautophagy and crinophagy as the means for intracellular degradation , 1981, Virchows Archiv. B, Cell pathology including molecular pathology.