Effects of Plant and Animal Natural Products on Mitophagy

Mitophagy is a protected cellular process that is essential for autophagic removal of damaged mitochondria and for preservation of a healthy mitochondrial population. In the last years, a particular interest has been devoted in studying the effects of natural compounds on mitophagy. Different natural compounds may modulate mitochondrial oxidative phosphorylation, the production of mitochondrial reactive oxygen species, the expression of mitophagy- and autophagy-related genes, and the activities of transcription factors which regulate the expression of mitochondrial proteins, thereby controlling mitochondrial damage and mitophagy. Remarkably, since mitochondrial function has a crucial role in the pathogenesis of various diseases (e.g., cancer, atherosclerosis, Duchenne muscular dystrophy, diabetes complications, Alzheimer's disease, and hepatic steatosis), these effects might have important therapeutic implications. In this review, preclinical studies investigating the role of different natural compounds in the modulation of mitophagy will be discussed.

[1]  C. E. Silva,et al.  Do dietary stresses affect the immune system of Periplaneta americana (Blattaria: Blattidae)? , 2020, Brazilian journal of biology = Revista brasleira de biologia.

[2]  R. Moreno-Sánchez,et al.  Resveratrol inhibits cancer cell proliferation by impairing oxidative phosphorylation and inducing oxidative stress , 2019, Toxicology and applied pharmacology.

[3]  Jun Zhang,et al.  To Explore the Protective Mechanism of PTEN-Induced Kinase 1 (PINK1)/Parkin Mitophagy-Mediated Extract of Periplaneta Americana on Lipopolysaccharide-Induced Cardiomyocyte Injury , 2019, Medical science monitor : international medical journal of experimental and clinical research.

[4]  Guoyu Pan,et al.  Enhanced Anti-diabetic Effect of Berberine Combined With Timosaponin B2 in Goto-Kakizaki Rats, Associated With Increased Variety and Exposure of Effective Substances Through Intestinal Absorption , 2019, Front. Pharmacol..

[5]  Chunchun Wang,et al.  Resveratrol improves intestinal barrier function, alleviates mitochondrial dysfunction and induces mitophagy in diquat challenged piglets1. , 2019, Food & function.

[6]  A. Sahebkar,et al.  Immune modulation by curcumin: The role of interleukin-10 , 2019, Critical reviews in food science and nutrition.

[7]  P. Maiti,et al.  Curcumin and Solid Lipid Curcumin Particles Induce Autophagy, but Inhibit Mitophagy and the PI3K-Akt/mTOR Pathway in Cultured Glioblastoma Cells , 2019, International journal of molecular sciences.

[8]  D. Francisci,et al.  NUtraceutical TReatment for hYpercholesterolemia in HIV-infected patients: The NU-TRY(HIV) randomized cross-over trial. , 2019, Atherosclerosis.

[9]  Y. Horio,et al.  Resveratrol Decreases Oxidative Stress by Restoring Mitophagy and Improves the Pathophysiology of Dystrophin-Deficient mdx Mice , 2018, Oxidative medicine and cellular longevity.

[10]  Y. Horio,et al.  Resveratrol Ameliorates Mitophagy Disturbance and Improves Cardiac Pathophysiology of Dystrophin-deficient mdx Mice , 2018, Scientific Reports.

[11]  Xu Wang,et al.  Berberine Ameliorates High Glucose-Induced Cardiomyocyte Injury via AMPK Signaling Activation to Stimulate Mitochondrial Biogenesis and Restore Autophagic Flux , 2018, Front. Pharmacol..

[12]  M. Boskabady,et al.  Curcumin affects tracheal responsiveness and lung pathology in asthmatic rats. , 2018 .

[13]  Yitao Wang,et al.  Periplaneta americana Ameliorates Dextran Sulfate Sodium-Induced Ulcerative Colitis in Rats by Keap1/Nrf-2 Activation, Intestinal Barrier Function, and Gut Microbiota Regulation , 2018, Front. Pharmacol..

[14]  Xiaoping Guo,et al.  Frataxin‐Mediated PINK1–Parkin‐Dependent Mitophagy in Hepatic Steatosis: The Protective Effects of Quercetin , 2018, Molecular nutrition & food research.

[15]  C. Hsieh,et al.  Aqueous extracts of Paeonia suffruticosa modulates mitochondrial proteostasis by reactive oxygen species-induced endoplasmic reticulum stress in pancreatic cancer cells. , 2018, Phytomedicine : international journal of phytotherapy and phytopharmacology.

[16]  Peng-Fei Wei,et al.  The Ethyl Acetate Extract of Gynura formosana Kitam. Leaves Inhibited Cervical Cancer Cell Proliferation via Induction of Autophagy , 2018, BioMed research international.

[17]  P. Han,et al.  Resveratrol Improves Muscle Atrophy by Modulating Mitochondrial Quality Control in STZ‐Induced Diabetic Mice , 2018, Molecular nutrition & food research.

[18]  S. Ryter,et al.  Quercetogetin protects against cigarette smoke extract-induced apoptosis in epithelial cells by inhibiting mitophagy. , 2018, Toxicology in vitro : an international journal published in association with BIBRA.

[19]  Lu Zhang,et al.  Anti-fibrotic role and mechanism of Periplaneta americana extracts in CCl4-induced hepatic fibrosis in rats , 2018, Acta biochimica et biophysica Sinica.

[20]  A. Sahebkar,et al.  Therapeutic effects of curcumin in inflammatory and immune‐mediated diseases: A nature‐made jack‐of‐all‐trades? , 2018, Journal of cellular physiology.

[21]  Tingting Li,et al.  Traditional herbal medicine-derived sulforaphene promotes mitophagic cell death in lymphoma cells through CRM1-mediated p62/SQSTM1 accumulation and AMPK activation. , 2018, Chemico-biological interactions.

[22]  Quan Liu,et al.  Toxicarioside H induces drug-resistant mitophagy via promoting expression of sirtuin-3 in lung cancer cells , 2018 .

[23]  Tianyue Jiang,et al.  Resveratrol attenuates oxidative damage through activating mitophagy in an in vitro model of Alzheimer's disease. , 2018, Toxicology letters.

[24]  Li-Chen Chen,et al.  Tomatidine Attenuates Airway Hyperresponsiveness and Inflammation by Suppressing Th2 Cytokines in a Mouse Model of Asthma , 2017, Mediators of inflammation.

[25]  G. E. Souza,et al.  Gastroprotective effect of the aqueous fraction of hydroacetonic leaf extract of Eugenia uniflora L. (Myrtaceae) (pitanga) against several gastric ulcer models in mice , 2017 .

[26]  Yu Zheng,et al.  Antioxidant Activity of Chinese Shanxi Aged Vinegar and Its Correlation with Polyphenols and Flavonoids During the Brewing Process. , 2017, Journal of food science.

[27]  A. Yang,et al.  Anti-tumor effects of the American cockroach, Periplaneta americana , 2017, Chinese Medicine.

[28]  J. Pedraza-Chaverri,et al.  Curcumin prevents cisplatin-induced renal alterations in mitochondrial bioenergetics and dynamic. , 2017, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[29]  Longping Wen,et al.  Antioxidant and anti-inflammatory activities of ethyl acetate extract of Gynura formosana (Kitam) leaves. , 2017, Experimental and therapeutic medicine.

[30]  Xu Song,et al.  Antiviral properties of resveratrol against pseudorabies virus are associated with the inhibition of IκB kinase activation , 2017, Scientific Reports.

[31]  L. Shang,et al.  Berberine containing quadruple therapy for initial Helicobacter pylori eradication , 2017, Medicine.

[32]  D. Spandidos,et al.  Anticancer and apoptosis-inducing effects of quercetin in vitro and in vivo , 2017, Oncology reports.

[33]  U. Förstermann,et al.  Antioxidant effects of resveratrol in the cardiovascular system , 2017, British journal of pharmacology.

[34]  C. Fu,et al.  Periplaneta americana Extracts Promote Skin Wound Healing via Nuclear Factor Kappa B Canonical Pathway and Extracellular Signal-Regulated Kinase Signaling , 2017, Evidence-based complementary and alternative medicine : eCAM.

[35]  M. Boskabady,et al.  Anti‐inflammatory, antioxidant, and immunomodulatory effects of curcumin in ovalbumin‐sensitized rat , 2017, BioFactors.

[36]  Amirhosein Sahebkar,et al.  Curcumin as a multifaceted compound against human papilloma virus infection and cervical cancers: A review of chemistry, cellular, molecular, and preclinical features , 2017, BioFactors.

[37]  M. Mattson,et al.  Tomatidine enhances lifespan and healthspan in C. elegans through mitophagy induction via the SKN-1/Nrf2 pathway , 2017, Scientific Reports.

[38]  M. M. Parisi,et al.  Autophagy induced by purple pitanga (Eugenia uniflora L.) extract triggered a cooperative effect on inducing the hepatic stellate cell death , 2016, Cell Biology and Toxicology.

[39]  Yu Zheng,et al.  Protective effects of Shanxi aged vinegar against hydrogen peroxide-induced oxidative damage in LO2 cells through Nrf2-mediated antioxidant responses , 2017 .

[40]  A. Sahebkar,et al.  Curcumin: A potentially powerful tool to reverse cisplatin‐induced toxicity , 2017, Pharmacological research.

[41]  Y. Panahi,et al.  Efficacy and Safety of Phytosomal Curcumin in Non-Alcoholic Fatty Liver Disease: A Randomized Controlled Trial , 2017, Drug Research.

[42]  M. Soukhtanloo,et al.  The effect of hydro-ethanolic extract of Curcuma longa rhizome and curcumin on total and differential WBC and serum oxidant, antioxidant biomarkers in rat model of asthma , 2017, Iranian journal of basic medical sciences.

[43]  A. Sahebkar,et al.  Curcumin as a natural regulator of monocyte chemoattractant protein-1. , 2017, Cytokine & growth factor reviews.

[44]  Bahman Emami,et al.  Relaxant effect of Curcuma longa on rat tracheal smooth muscle and its possible mechanisms , 2017, Pharmaceutical biology.

[45]  Baoguo Sun,et al.  Aroma Constituents in Shanxi Aged Vinegar before and after Aging. , 2016, Journal of agricultural and food chemistry.

[46]  Ming Zhang,et al.  Therapeutic Potential and Mechanisms of Berberine in Cardiovascular Disease , 2016, Current Pharmacology Reports.

[47]  D. Shangguan,et al.  A Cyanine Dye to Probe Mitophagy: Simultaneous Detection of Mitochondria and Autolysosomes in Live Cells. , 2016, Journal of the American Chemical Society.

[48]  A. Sahebkar,et al.  The effects of a nutraceutical combination on plasma lipids and glucose: A systematic review and meta-analysis of randomized controlled trials. , 2016, Pharmacological research.

[49]  A. Zanchetti,et al.  Effects of Quercetin on Blood Pressure: A Systematic Review and Meta‐Analysis of Randomized Controlled Trials , 2016, Journal of the American Heart Association.

[50]  B. Cavalcanti,et al.  Berberine Antifungal Activity in Fluconazole-Resistant Pathogenic Yeasts: Action Mechanism Evaluated by Flow Cytometry and Biofilm Growth Inhibition in Candida spp. , 2016, Antimicrobial Agents and Chemotherapy.

[51]  Jian Zhang,et al.  The role of Resveratrol-induced mitophagy/autophagy in peritoneal mesothelial cells inflammatory injury via NLRP3 inflammasome activation triggered by mitochondrial ROS. , 2016, Experimental cell research.

[52]  Liegang Liu,et al.  Quercetin Attenuates Chronic Ethanol-Induced Hepatic Mitochondrial Damage through Enhanced Mitophagy , 2016, Nutrients.

[53]  Ping Yang,et al.  Hypoglycemic activities of lyophilized powder of Gynura divaricata by improving antioxidant potential and insulin signaling in type 2 diabetic mice , 2015, Food & nutrition research.

[54]  K. Borges,et al.  Sulforaphane is anticonvulsant and improves mitochondrial function , 2015, Journal of neurochemistry.

[55]  P. Petit,et al.  Curcumin induces crosstalk between autophagy and apoptosis mediated by calcium release from the endoplasmic reticulum, lysosomal destabilization and mitochondrial events , 2015, Cell Death Discovery.

[56]  J. Fahey,et al.  Sulforaphane improves the bronchoprotective response in asthmatics through Nrf2-mediated gene pathways , 2015, Respiratory Research.

[57]  A. Cossarizza,et al.  Natural Compounds Modulating Mitochondrial Functions , 2015, Evidence-based complementary and alternative medicine : eCAM.

[58]  Xu Song,et al.  Antibacterial activity and mechanism of berberine against Streptococcus agalactiae. , 2015, International journal of clinical and experimental pathology.

[59]  A. L. Oliveira,et al.  Study of supercritical extraction from Brazilian cherry seeds (Eugenia uniflora L.) with bioactive compounds , 2015 .

[60]  K. James,et al.  Elucidation of the Mass Fragmentation Pathways of Tomatidine and β1-Hydroxytomatine using Orbitrap Mass Spectrometry , 2015, Natural product communications.

[61]  F. Guma,et al.  The Interplay Between Apoptosis, Mitophagy and Mitochondrial Biogenesis Induced by Resveratrol Can Determine Activated Hepatic Stellate Cells Death or Survival , 2015, Cell Biochemistry and Biophysics.

[62]  Jianjun Gao,et al.  Anti-tumor effects and cellular mechanisms of resveratrol. , 2015, Drug discoveries & therapeutics.

[63]  M. Pu,et al.  Sulforaphane Protects Rodent Retinas against Ischemia-Reperfusion Injury through the Activation of the Nrf2/HO-1 Antioxidant Pathway , 2014, PloS one.

[64]  Lei Yang,et al.  Possible antioxidant mechanism of melanoidins extract from Shanxi aged vinegar in mitophagy-dependent and mitophagy-independent pathways. , 2014, Journal of agricultural and food chemistry.

[65]  G. Mitchell,et al.  Unraveling the structure-activity relationship of tomatidine, a steroid alkaloid with unique antibiotic properties against persistent forms of Staphylococcus aureus. , 2014, European journal of medicinal chemistry.

[66]  Steven D. Kunkel,et al.  Systems-based Discovery of Tomatidine as a Natural Small Molecule Inhibitor of Skeletal Muscle Atrophy* , 2014, The Journal of Biological Chemistry.

[67]  Jian-Dong Jiang,et al.  Antioxidant and Anti-Inflammatory Activities of Berberine in the Treatment of Diabetes Mellitus , 2014, Evidence-based complementary and alternative medicine : eCAM.

[68]  Hui-Ting Lin,et al.  Tomatidine inhibits invasion of human lung adenocarcinoma cell A549 by reducing matrix metalloproteinases expression. , 2013, Chemico-biological interactions.

[69]  M. Duchen,et al.  Cellular and molecular mechanisms of mitochondrial function , 2012, Best practice & research. Clinical endocrinology & metabolism.

[70]  L. Savegnago,et al.  Essential oil of the leaves of Eugenia uniflora L.: antioxidant and antimicrobial properties. , 2012, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[71]  Xiao-Ming Yin,et al.  Mitophagy: mechanisms, pathophysiological roles, and analysis , 2012, Biological chemistry.

[72]  P. Nick,et al.  The Phytoalexin Resveratrol Regulates the Initiation of Hypersensitive Cell Death in Vitis Cell , 2011, PloS one.

[73]  Tzung-Han Chou,et al.  Antioxidant and Antimelanogenic Behaviors of Paeonia suffruticosa , 2011, Plant foods for human nutrition.

[74]  D. Klionsky,et al.  Mitochondria removal by autophagy , 2011, Autophagy.

[75]  A. Sahebkar.  Molecular mechanisms for curcumin benefits against ischemic injury. , 2010, Fertility and sterility.

[76]  S. Kuo,et al.  Cardiac glycosides from Antiaris toxicaria with potent cardiotonic activity. , 2010, Journal of natural products.

[77]  C. Rezende,et al.  Antinociceptive and hypothermic evaluation of the leaf essential oil and isolated terpenoids from Eugenia uniflora L. (Brazilian Pitanga). , 2009, Phytomedicine : international journal of phytotherapy and phytopharmacology.

[78]  Wenli Mei,et al.  A New Cytotoxic 19-Nor-cardenolide from the Latex of Antiaris toxicaria , 2009, Molecules.

[79]  Midori Takasaki,et al.  Cancer chemopreventive activity of the prenylated coumarin, umbelliprenin, in vivo , 2009, European journal of cancer prevention : the official journal of the European Cancer Prevention Organisation.

[80]  K. Fung,et al.  Traditional Chinese medicine for atopic eczema: PentaHerbs formula suppresses inflammatory mediators release from mast cells. , 2008, Journal of ethnopharmacology.

[81]  Jen-kun Lin,et al.  Tomatidine inhibits iNOS and COX‐2 through suppression of NF‐κB and JNK pathways in LPS‐stimulated mouse macrophages , 2008, FEBS letters.

[82]  J. Duke.  Duke's Handbook of Medicinal Plants of Latin America , 2007 .

[83]  Jin-Bao Ma,et al.  [Protection of polysaccharides-2b from mudan cortex of Paeonia suffruticosa andr on diabetic cataract in rats]. , 2007, Zhongguo Zhong yao za zhi = Zhongguo zhongyao zazhi = China journal of Chinese materia medica.

[84]  D. Barreca,et al.  Flavonoid composition of Citrus juices. , 2007, Molecules.

[85]  Vijay L Kumar,et al.  Anticancer and cytotoxic properties of the latex of Calotropis procera in a transgenic mouse model of hepatocellular carcinoma. , 2006, World journal of gastroenterology.

[86]  Mei-Hsien Lee,et al.  The phenolic constituents and free radical scavenging activities of Gynura formosana Kiamnra , 2005 .

[87]  J. J. Sung,et al.  Chemoprevention of gastric cancer by celecoxib in rats , 2004, Gut.

[88]  D. Witt,et al.  Resveratrol: Phytoestrogen Effects on Reproductive Physiology and Behavior in Female Rats , 2002, Hormones and Behavior.

[89]  M B Katan,et al.  Dietary flavonoids: intake, health effects and bioavailability. , 1999, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[90]  H. C. Lin,et al.  Two novel compounds from Paeonia suffructicosa. , 1998, Journal of natural products.

[91]  W. H. Lewis,et al.  Mitochondria (and other cytoplasmic structures) in tissue cultures , 1915 .

[92]  F. Bernini,et al.  Joint position statement on "Nutraceuticals for the treatment of hypercholesterolemia" of the Italian Society of Diabetology (SID) and of the Italian Society for the Study of Arteriosclerosis (SISA). , 2017, Nutrition, metabolism, and cardiovascular diseases : NMCD.

[93]  Yu Zheng,et al.  Shanxi aged vinegar against hydrogen peroxide-induced oxidative damage in LO 2 cells through Nrf 2-mediated antioxidant responses , 2017 .

[94]  Mohammed Akbar,et al.  The Benefits of Natural Products for Neurodegenerative Diseases , 2016, Advances in Neurobiology.

[95]  Xixin Yan,et al.  Sulforaphane exerts anti-inflammatory effects against lipopolysaccharide-induced acute lung injury in mice through the Nrf2/ARE pathway. , 2016, International journal of molecular medicine.

[96]  Chuanshan Xu,et al.  TEM observation of ultrasound-induced mitophagy in nasopharyngeal carcinoma cells in the presence of curcumin. , 2012, Experimental and therapeutic medicine.

[97]  R. Youle,et al.  Mechanisms of mitophagy , 2010, Nature Reviews Molecular Cell Biology.

[98]  Chi-Tang Ho,et al.  Polymethoxyflavones : Chemistry, Biological Activity, and Occurrence in Orange Peel , 2008 .