TY - JOUR
T1 - Preparation for oxidative stress under hypoxia and metabolic depression
T2 - Revisiting the proposal two decades later
AU - Hermes-Lima, Marcelo
AU - Moreira, Daniel C.
AU - Rivera-Ingraham, Georgina A.
AU - Giraud-Billoud, Maximiliano
AU - Genaro-Mattos, Thiago C.
AU - Campos, Élida G.
N1 - Funding Information:
This work was supported by grants from INCT-Processos Redox em Biomedicina (CNPq, Brazil), Projeto Universal (CNPq) and from the Fundação de Amparo à Pesquisa do Distrito Federal (FAPDF, Grant 193.000.040/2012 ). D.C. Moreira is a graduate student funded by a CAPES studentship. M. Hermes-Lima receives a Research Fellowship from CNPq. G. Rivera-Ingraham is supported by Marie Curie Actions EU grant ( FP7-PEOPLE-2013-IEF ) [Grant 622087-“IAS-Life” ]. We acknowledge Prof. Alexis F. Welker (University of Brasília) for the critical reading of the manuscript. This study is in honor of Cláudio Mário Guimarães da Silva (Rio de Janeiro, Brazil), retired biology teacher.
Publisher Copyright:
© 2015 Elsevier Inc.
PY - 2015/12/1
Y1 - 2015/12/1
N2 - Organisms that tolerate wide variations in oxygen availability, especially to hypoxia, usually face harsh environmental conditions during their lives. Such conditions include, for example, lack of food and/or water, low or high temperatures, and reduced oxygen availability. In contrast to an expected strong suppression of protein synthesis, a great number of these animals present increased levels of antioxidant defenses during oxygen deprivation. These observations have puzzled researchers for more than 20 years. Initially, two predominant ideas seemed to be irreconcilable: on one hand, hypoxia would decrease reactive oxygen species (ROS) production, while on the other the induction of antioxidant enzymes would require the overproduction of ROS. This induction of antioxidant enzymes during hypoxia was viewed as a way to prepare animals for oxidative damage that may happen ultimately during reoxygenation. The term preparation for oxidative stress (POS) was coined in 1998 based on such premise. However, there are many cases of increased oxidative damage in several hypoxia-tolerant organisms under hypoxia. In addition, over the years, the idea of an assured decrease in ROS formation under hypoxia was challenged. Instead, several findings indicate that the production of ROS actually increases in response to hypoxia. Recently, it became possible to provide a comprehensive explanation for the induction of antioxidant enzymes under hypoxia. The supporting evidence and the limitations of the POS idea are extensively explored in this review as we discuss results from research on estivation and situations of low oxygen stress, such as hypoxia, freezing exposure, severe dehydration, and air exposure of water-breathing animals. We propose that, under some level of oxygen deprivation, ROS are overproduced and induce changes leading to hypoxic biochemical responses. These responses would occur mainly through the activation of specific transcription factors (FoxO, Nrf2, HIF-1, NF-κB, and p53) and post translational mechanisms, both mechanisms leading to enhanced antioxidant defenses. Moreover, reactive nitrogen species are candidate modulators of ROS generation in this scenario. We conclude by drawing out the future perspectives in this field of research, and how advances in the knowledge of the mechanisms involved in the POS strategy will offer new and innovative study scenarios of biological and physiological cellular responses to environmental stress.
AB - Organisms that tolerate wide variations in oxygen availability, especially to hypoxia, usually face harsh environmental conditions during their lives. Such conditions include, for example, lack of food and/or water, low or high temperatures, and reduced oxygen availability. In contrast to an expected strong suppression of protein synthesis, a great number of these animals present increased levels of antioxidant defenses during oxygen deprivation. These observations have puzzled researchers for more than 20 years. Initially, two predominant ideas seemed to be irreconcilable: on one hand, hypoxia would decrease reactive oxygen species (ROS) production, while on the other the induction of antioxidant enzymes would require the overproduction of ROS. This induction of antioxidant enzymes during hypoxia was viewed as a way to prepare animals for oxidative damage that may happen ultimately during reoxygenation. The term preparation for oxidative stress (POS) was coined in 1998 based on such premise. However, there are many cases of increased oxidative damage in several hypoxia-tolerant organisms under hypoxia. In addition, over the years, the idea of an assured decrease in ROS formation under hypoxia was challenged. Instead, several findings indicate that the production of ROS actually increases in response to hypoxia. Recently, it became possible to provide a comprehensive explanation for the induction of antioxidant enzymes under hypoxia. The supporting evidence and the limitations of the POS idea are extensively explored in this review as we discuss results from research on estivation and situations of low oxygen stress, such as hypoxia, freezing exposure, severe dehydration, and air exposure of water-breathing animals. We propose that, under some level of oxygen deprivation, ROS are overproduced and induce changes leading to hypoxic biochemical responses. These responses would occur mainly through the activation of specific transcription factors (FoxO, Nrf2, HIF-1, NF-κB, and p53) and post translational mechanisms, both mechanisms leading to enhanced antioxidant defenses. Moreover, reactive nitrogen species are candidate modulators of ROS generation in this scenario. We conclude by drawing out the future perspectives in this field of research, and how advances in the knowledge of the mechanisms involved in the POS strategy will offer new and innovative study scenarios of biological and physiological cellular responses to environmental stress.
KW - Anoxia
KW - Dehydration
KW - Estivation
KW - Freeze tolerance
KW - Hypoxia tolerance
KW - Ischemia
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U2 - 10.1016/j.freeradbiomed.2015.07.156
DO - 10.1016/j.freeradbiomed.2015.07.156
M3 - Review article
C2 - 26408245
AN - SCOPUS:84946593511
SN - 0891-5849
VL - 89
SP - 1122
EP - 1143
JO - Free Radical Biology and Medicine
JF - Free Radical Biology and Medicine
ER -