Altered dynamics of mitochondria and reactive oxygen species in the erythrocytes of migrating red-headed buntings

Background: Blood antioxidants provide propensity to mitigate reactive oxygen species (ROS) apart from other oxidative challenges during a high-energy state of migration in night migratory songbirds. The study investigated the modulation of erythrocytes, mitochondrial abundance, hematocrit changes, and relative expression of fat transport-related genes during migration in red-headed buntings (Emberiza bruniceps). We hypothesized an increase in antioxidants along with the mitigation of mitochondria-related reactive oxygen species elevation and consequential apoptosis occurring during migration. Methods: Male red-headed buntings (n = 6) were placed under short days (8 h of light and 16 h of dark, 8L:16D)/long days (14L:10D) and photo induced to simulated non-migratory, nMig; pre-migratory, pMig; and migratory, Mig, states. Erythrocyte shape, reactive oxygen species production, mitochondrial membrane potential (MMP), reticulocyte proportion, and apoptosis were analyzed using flow cytometry and relative expression of fat metabolizing and antioxidant genes was measured by using qPCR. Results: There was a significant increase in hematocrit, erythrocyte area, and mitochondrial membrane potential. Reactive oxygen species and apoptotic erythrocyte proportion declined in the Mig state. The changes in antioxidant genes (SOD1 and NOS2), fatty acid translocase (CD36), and metabolic (FABP3, DGAT2, GOT2, and ATGL) genes showed a significant increment during the Mig state. Conclusion: These results suggested that adaptive changes occur in mitochondrial behavior and apoptosis of erythrocytes. The transition in erythrocytes, antioxidant genes, and fatty acid metabolism gene expressions suggested differences in regulatory strategies at the cellular/transcriptional level during different states of simulated migration in birds.

[1]  N. Bhardwaj,et al.  Aflatoxin B1 administration induces reactive oxygen species production and apoptosis of erythrocytes in mice. , 2022, Toxicon : official journal of the International Society on Toxinology.

[2]  J. Ramos,et al.  Blood Metabolites and Profiling Stored Adipose Tissue Reveal the Differential Migratory Strategies of Eurasian Reed and Sedge Warblers , 2022, Birds.

[3]  S. Bearhop,et al.  Changes in Behaviour and Proxies of Physiology Suggest Individual Variation in the Building of Migratory Phenotypes in Preparation for Long-Distance Flights , 2022, Frontiers in Ecology and Evolution.

[4]  S. McWilliams,et al.  How Birds During Migration Maintain (Oxidative) Balance , 2021, Frontiers in Ecology and Evolution.

[5]  C. Soulsbury,et al.  Energetic Lifestyle Drives Size and Shape of Avian Erythrocytes , 2021, Integrative and comparative biology.

[6]  M. Hau,et al.  Inferring Whole-Organism Metabolic Rate From Red Blood Cells in Birds , 2021, Frontiers in Physiology.

[7]  S. K. Bhardwaj,et al.  Molecular changes associated with migratory departure from wintering areas in obligate songbird migrants. , 2021, The Journal of experimental biology.

[8]  R. Arya,et al.  Night Migratory Songbirds Exhibit Metabolic Ability to Support High Aerobic Capacity during Migration , 2020, ACS omega.

[9]  S. Knaga,et al.  Early morphological and apoptotic responses of bird erythrocytes to thermal stress , 2020, Biotechnic & histochemistry : official publication of the Biological Stain Commission.

[10]  S. DuRant,et al.  Fluorescent Heme Degradation Products Are Biomarkers of Oxidative Stress and Linked to Impaired Membrane Integrity in Avian Red Blood Cells , 2020, Physiological and Biochemical Zoology.

[11]  Mark T Gladwin,et al.  Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation , 2019, Physiological reviews.

[12]  D. Lacombe,et al.  Ubiquitin-Dependent Degradation of Mitochondrial Proteins Regulates Energy Metabolism. , 2018, Cell reports.

[13]  N. Bhardwaj,et al.  Paraquat treatment modulates integrin associated protein (CD47) and basigin (CD147) expression and mitochondrial potential on erythroid cells in mice. , 2018, Environmental toxicology and pharmacology.

[14]  Patrick J Butler,et al.  The physiological basis of bird flight , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[15]  N. J. Gupta,et al.  Seasonal modulation of diurnal food consumption in Indian songbirds , 2016 .

[16]  A. Hoffman,et al.  Comparison of the effects of glycerol, dimethyl sulfoxide, and hydroxyethyl starch solutions for cryopreservation of avian red blood cells. , 2015, American journal of veterinary research.

[17]  N. Bhardwaj,et al.  Selective loss of younger erythrocytes from blood circulation and changes in erythropoietic patterns in bone marrow and spleen in mouse anemia induced by poly-dispersed single-walled carbon nanotubes , 2015, Nanotoxicology.

[18]  P. Minias.  The use of haemoglobin concentrations to assess physiological condition in birds: a review , 2015, Conservation physiology.

[19]  C. Winterbourn.  Are free radicals involved in thiol-based redox signaling? , 2015, Free radical biology & medicine.

[20]  S. Rani,et al.  Annual Life History–Dependent Gene Expression in the Hypothalamus and Liver of a Migratory Songbird , 2014, Journal of biological rhythms.

[21]  S. Sollott,et al.  Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. , 2014, Physiological reviews.

[22]  N. Bhardwaj,et al.  Elimination of Young Erythrocytes from Blood Circulation and Altered Erythropoietic Patterns during Paraquat Induced Anemic Phase in Mice , 2014, PloS one.

[23]  D. Costantini,et al.  Oxidative Stress in Endurance Flight: An Unconsidered Factor in Bird Migration , 2014, PloS one.

[24]  S. Rani,et al.  Daily Expression of Six Clock Genes in Central and Peripheral Tissues of a Night-Migratory SongBird: Evidence for Tissue-Specific Circadian Timing , 2013, Chronobiology international.

[25]  J. Zoll,et al.  Avian erythrocytes have functional mitochondria, opening novel perspectives for birds as animal models in the study of ageing , 2013, Frontiers in Zoology.

[26]  Vinod Kumar,et al.  Testes play a role in termination but not in initiation of the spring migration in the night-migratory blackheaded bunting , 2013 .

[27]  A. J. Hulbert,et al.  Does the oxidative stress theory of aging explain longevity differences in birds? I. Mitochondrial ROS production , 2012, Experimental Gerontology.

[28]  C. Guglielmo,et al.  Migration- and exercise-induced changes to flight muscle size in migratory birds and association with IGF1 and myostatin mRNA expression , 2011, Journal of Experimental Biology.

[29]  B. Halliwell.  Free radicals and antioxidants - quo vadis? , 2011, Trends in pharmacological sciences.

[30]  C. Guglielmo.  Move that fatty acid: fuel selection and transport in migratory birds and bats. , 2010, Integrative and comparative biology.

[31]  P. Butler.  High fliers: the physiology of bar-headed geese. , 2010, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[32]  R. Youle,et al.  The role of mitochondria in apoptosis*. , 2009, Annual review of genetics.

[33]  Seon-Yong Jeong,et al.  The role of mitochondria in apoptosis. , 2008, BMB reports.

[34]  J. Bańbura,et al.  Habitat and year-to-year variation in haemoglobin concentration in nestling blue tits Cyanistes caeruleus. , 2007, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[35]  Brandon L. Pearson,et al.  Sources of variation in haematocrit in birds , 2007 .

[36]  A. Bruce-Keller,et al.  SOD1 overexpression alters ROS production and reduces neurotoxic inflammatory signaling in microglial cells , 2007, Journal of Neuroimmunology.

[37]  V. Kumar,et al.  Changes in food intake, body weight, gonads and plasma concentrations of thyroxine, luteinizing hormone and testosterone in captive male buntings exposed to natural daylengths at 29° N , 1995, Journal of Biosciences.

[38]  F. Spina,et al.  Effect of endurance flight on haematocrit in migrating birds , 2006, Journal of Ornithology.

[39]  Michael Karin,et al.  Reactive Oxygen Species Promote TNFα-Induced Death and Sustained JNK Activation by Inhibiting MAP Kinase Phosphatases , 2005, Cell.

[40]  N. Abumrad,et al.  Role of CD36 in membrane transport of long-chain fatty acids , 2002, Current opinion in clinical nutrition and metabolic care.

[41]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[42]  A. Bonen,et al.  Muscle-specific Overexpression of FAT/CD36 Enhances Fatty Acid Oxidation by Contracting Muscle, Reduces Plasma Triglycerides and Fatty Acids, and Increases Plasma Glucose and Insulin* , 1999, The Journal of Biological Chemistry.

[43]  A. Kostelecka-Myrcha.  The Ratio of Amount of Haemoglobin to Total Surface Area of Erythrocytes in Birds in Relation to Body Mass, Age of Nestlings, and Season of the Year , 1997, Physiological Zoology.

[44]  T. Piersma,et al.  Build-up of Red Blood Cells in Refuelling Bar-Tailed Godwits in Relation to Individual Migratory Quality , 1996 .

[45]  J. Merilä,et al.  Fat Reserves and Health State in Migrant Goldcrest Regulus regulus , 1995 .

[46]  S. Snyder,et al.  Nitric oxide: a physiologic messenger molecule. , 1994, Annual review of biochemistry.

[47]  H. Beug,et al.  Primitive series embryonic chick erythrocytes express the transferrin receptor. , 1986, Experimental cell research.