Avian erythrocytes have functional mitochondria, opening novel perspectives for birds as animal models in the study of ageing

Antoine Stier*, Pierre Bize, Quentin Schull, Joffrey Zoll, Francois Singh, Bernard Geny, Frederic Gros, Cathy Royer, Sylvie Massemin, Francois Criscuolo

*Corresponding author for this work

Research output: Contribution to journalArticle

38 Citations (Scopus)

Abstract

Background: In contrast to mammalian erythrocytes, which have lost their nucleus and mitochondria during maturation, the erythrocytes of almost all other vertebrate species are nucleated throughout their lifespan. Little research has been done however to test for the presence and functionality of mitochondria in these cells, especially for birds. Here, we investigated those two points in erythrocytes of one common avian model: the zebra finch (Taeniopygia guttata).

Results: Transmission electron microscopy showed the presence of mitochondria in erythrocytes of this small passerine bird, especially after removal of haemoglobin interferences. High-resolution respirometry revealed increased or decreased rates of oxygen consumption by erythrocytes in response to the addition of respiratory chain substrates or inhibitors, respectively. Fluorometric assays confirmed the production of mitochondrial superoxide by avian erythrocytes. Interestingly, measurements of plasmatic oxidative markers indicated lower oxidative stress in blood of the zebra finch compared to a size-matched mammalian model, the mouse.

Conclusions: Altogether, those findings demonstrate that avian erythrocytes possess functional mitochondria in terms of respiratory activities and reactive oxygen species (ROS) production. Interestingly, since blood oxidative stress was lower for our avian model compared to a size-matched mammalian, our results also challenge the idea that mitochondrial ROS production could have been one actor leading to this loss during the course of evolution. Opportunities to assess mitochondrial functioning in avian erythrocytes open new perspectives in the use of birds as models for longitudinal studies of ageing via lifelong blood sampling of the same subjects.

Original languageEnglish
Article number33
Number of pages9
JournalFrontiers in zoology
Volume10
DOIs
Publication statusPublished - 8 Jun 2013

Keywords

  • Red blood cell
  • Ageing
  • Mitochondria
  • ROS
  • Oxidative stress
  • Electron transport chain
  • RED-BLOOD-CELLS
  • OXIDATIVE STRESS
  • RAINBOW-TROUT
  • FREE-RADICALS
  • PERIPHERAL-BLOOD
  • FINE-STRUCTURE
  • LIFE-SPAN
  • DEATH
  • MEMBRANE
  • PIGEON

Cite this

Avian erythrocytes have functional mitochondria, opening novel perspectives for birds as animal models in the study of ageing. / Stier, Antoine; Bize, Pierre; Schull, Quentin; Zoll, Joffrey; Singh, Francois; Geny, Bernard; Gros, Frederic; Royer, Cathy; Massemin, Sylvie; Criscuolo, Francois.

In: Frontiers in zoology, Vol. 10, 33, 08.06.2013.

Research output: Contribution to journalArticle

Stier, Antoine ; Bize, Pierre ; Schull, Quentin ; Zoll, Joffrey ; Singh, Francois ; Geny, Bernard ; Gros, Frederic ; Royer, Cathy ; Massemin, Sylvie ; Criscuolo, Francois. / Avian erythrocytes have functional mitochondria, opening novel perspectives for birds as animal models in the study of ageing. In: Frontiers in zoology. 2013 ; Vol. 10.
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abstract = "Background: In contrast to mammalian erythrocytes, which have lost their nucleus and mitochondria during maturation, the erythrocytes of almost all other vertebrate species are nucleated throughout their lifespan. Little research has been done however to test for the presence and functionality of mitochondria in these cells, especially for birds. Here, we investigated those two points in erythrocytes of one common avian model: the zebra finch (Taeniopygia guttata).Results: Transmission electron microscopy showed the presence of mitochondria in erythrocytes of this small passerine bird, especially after removal of haemoglobin interferences. High-resolution respirometry revealed increased or decreased rates of oxygen consumption by erythrocytes in response to the addition of respiratory chain substrates or inhibitors, respectively. Fluorometric assays confirmed the production of mitochondrial superoxide by avian erythrocytes. Interestingly, measurements of plasmatic oxidative markers indicated lower oxidative stress in blood of the zebra finch compared to a size-matched mammalian model, the mouse.Conclusions: Altogether, those findings demonstrate that avian erythrocytes possess functional mitochondria in terms of respiratory activities and reactive oxygen species (ROS) production. Interestingly, since blood oxidative stress was lower for our avian model compared to a size-matched mammalian, our results also challenge the idea that mitochondrial ROS production could have been one actor leading to this loss during the course of evolution. Opportunities to assess mitochondrial functioning in avian erythrocytes open new perspectives in the use of birds as models for longitudinal studies of ageing via lifelong blood sampling of the same subjects.",
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AU - Stier, Antoine

AU - Bize, Pierre

AU - Schull, Quentin

AU - Zoll, Joffrey

AU - Singh, Francois

AU - Geny, Bernard

AU - Gros, Frederic

AU - Royer, Cathy

AU - Massemin, Sylvie

AU - Criscuolo, Francois

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N2 - Background: In contrast to mammalian erythrocytes, which have lost their nucleus and mitochondria during maturation, the erythrocytes of almost all other vertebrate species are nucleated throughout their lifespan. Little research has been done however to test for the presence and functionality of mitochondria in these cells, especially for birds. Here, we investigated those two points in erythrocytes of one common avian model: the zebra finch (Taeniopygia guttata).Results: Transmission electron microscopy showed the presence of mitochondria in erythrocytes of this small passerine bird, especially after removal of haemoglobin interferences. High-resolution respirometry revealed increased or decreased rates of oxygen consumption by erythrocytes in response to the addition of respiratory chain substrates or inhibitors, respectively. Fluorometric assays confirmed the production of mitochondrial superoxide by avian erythrocytes. Interestingly, measurements of plasmatic oxidative markers indicated lower oxidative stress in blood of the zebra finch compared to a size-matched mammalian model, the mouse.Conclusions: Altogether, those findings demonstrate that avian erythrocytes possess functional mitochondria in terms of respiratory activities and reactive oxygen species (ROS) production. Interestingly, since blood oxidative stress was lower for our avian model compared to a size-matched mammalian, our results also challenge the idea that mitochondrial ROS production could have been one actor leading to this loss during the course of evolution. Opportunities to assess mitochondrial functioning in avian erythrocytes open new perspectives in the use of birds as models for longitudinal studies of ageing via lifelong blood sampling of the same subjects.

AB - Background: In contrast to mammalian erythrocytes, which have lost their nucleus and mitochondria during maturation, the erythrocytes of almost all other vertebrate species are nucleated throughout their lifespan. Little research has been done however to test for the presence and functionality of mitochondria in these cells, especially for birds. Here, we investigated those two points in erythrocytes of one common avian model: the zebra finch (Taeniopygia guttata).Results: Transmission electron microscopy showed the presence of mitochondria in erythrocytes of this small passerine bird, especially after removal of haemoglobin interferences. High-resolution respirometry revealed increased or decreased rates of oxygen consumption by erythrocytes in response to the addition of respiratory chain substrates or inhibitors, respectively. Fluorometric assays confirmed the production of mitochondrial superoxide by avian erythrocytes. Interestingly, measurements of plasmatic oxidative markers indicated lower oxidative stress in blood of the zebra finch compared to a size-matched mammalian model, the mouse.Conclusions: Altogether, those findings demonstrate that avian erythrocytes possess functional mitochondria in terms of respiratory activities and reactive oxygen species (ROS) production. Interestingly, since blood oxidative stress was lower for our avian model compared to a size-matched mammalian, our results also challenge the idea that mitochondrial ROS production could have been one actor leading to this loss during the course of evolution. Opportunities to assess mitochondrial functioning in avian erythrocytes open new perspectives in the use of birds as models for longitudinal studies of ageing via lifelong blood sampling of the same subjects.

KW - Red blood cell

KW - Ageing

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KW - Oxidative stress

KW - Electron transport chain

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KW - OXIDATIVE STRESS

KW - RAINBOW-TROUT

KW - FREE-RADICALS

KW - PERIPHERAL-BLOOD

KW - FINE-STRUCTURE

KW - LIFE-SPAN

KW - DEATH

KW - MEMBRANE

KW - PIGEON

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JO - Frontiers in zoology

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