Hypoxic incubation blunts the development of thermogenesis in chicken embryos and hatchlings

Azzam, Milène A.; Szdzuy, Kirsten; Mortola, Jacopo P.

doi:10.1152/ajpregu.00885.2006

Cited by 29 publications

(15 citation statements)

References 39 publications

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“…Presumably, the reluctance of Hx to drop V O 2 in hypoxia reflected the need to pay back some lactic acid accumulation and O 2 debt contracted during the hatching effort or the compensatory catch-up growth on return to normoxia. In fact, a small tendency to maintain a higher resting V O 2 was detectable also in normoxia, and it was observed in previous experiments on 1-day-old hatchlings after hypoxic incubation (1). Also, the hypoxia-induced catecholamine release could help the Hx hatchlings to maintain V O 2 in hypoxia (45).…”

Section: Discussionsupporting

confidence: 61%

“…In resting conditions, the V O 2 of the hatchlings (0.76 ml/min or ϳ19 ml⅐kg Ϫ1 ⅐min Ϫ1 ) corresponded to what should be expected at 38°C (1,25,28). The V E/V O 2 of ϳ22 was low compared with newborn or adult mammals of similar body size (24) but was quite similar to the V E/V O 2 values of 21-22 of adult birds (2,43), including the domestic fowl (6).…”

Section: Discussionsupporting

confidence: 55%

“…Hx group: resting conditions. Embryonic hypoxia is known to decrease body growth; however, the additional 10 -12 h of incubation allow the Hx embryos to incorporate the remaining yolk and reach a body weight similar to that of Nx (1). At that time, in resting conditions, there were virtually no differences in metabolic and breathing parameters between Hx and Nx hatchlings, except for a slightly higher V E (and V E/V O 2 ) in Hx (Table 1).…”

Section: Discussionmentioning

confidence: 97%

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Ventilatory chemosensitivity of the 1-day-old chicken hatchling after embryonic hypoxia

Szdzuy

Mortola²

2007

American Journal of Physiology-Regulatory, Integrative and Comp

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Szdzuy K, Mortola JP. Ventilatory chemosensitivity of the 1-dayold chicken hatchling after embryonic hypoxia. Am J Physiol Regul Integr Comp Physiol 293: R1640-R1649, 2007. First published August 8, 2007; doi:10.1152/ajpregu.00422.2007.-We investigated the effects of sustained embryonic hypoxia on the neonatal ventilatory chemosensitivity. White Leghorn chicken eggs were incubated at 38°C either in 21% O 2 throughout incubation (normoxia, Nx) or in 15% O 2 from embryonic day 5 (hypoxia, Hx), hatching time included. Hx embryos hatched ϳ11 h later than Nx, with similar body weights. Measurements of gaseous metabolism (oxygen consumption, V O2) and pulmonary ventilation (V E) were conducted either within the first 8 h (early) or later hours (late) of the first posthatching day. In resting conditions, Hx had similar V O2 and body temperature (Tb) and slightly higher V E and ventilatory equivalent (V E/V O2) than Nx. Ventilatory chemosensitivity was evaluated from the degree of hyperpnea (increase in V E) and of hyperventilation (increase in V E/V O2) during acute hypoxia (15 and 10% O2, 20 min each) and acute hypercapnia (2 and 4% CO2, 20 min each). The chemosensitivity differed between the early and late hours, and at either time the responses to hypoxia and hypercapnia were less in Hx than in Nx because of a lower increase in V E and a lower hypoxic hypometabolism. In a second group of Nx and Hx hatchlings, the V E response to 10% O2 was tested in the same hatchlings at the early and late hours. The results confirmed the lower hypoxic chemosensitivity of Hx. We conclude that hypoxic incubation affected the development of respiratory control, resulting in a blunted ventilatory chemosensitivity. developmental plasticity; epigenetic adaptation; hypercapnia; hypometabolism; hypoxic ventilatory response IN MAMMALS AND BIRDS, the development of the respiratory system is a long process. It begins early during gestation or incubation, when the embryo's gas-exchange needs are provided by nonpulmonary organs, and continues far into postnatal life, when pulmonary ventilation is the only means of fulfilling the aerobic requirements of the growing organism. A question of both biological and clinical interest is whether or not this process is strictly under genetic control or can be modulated by external events. In this latter case, the rather long time for structural and functional development gives the respiratory system the opportunity of adjusting to the postnatal changes in metabolic needs. Equally, however, it opens a potentially risky time window for environmental factors to interfere negatively with the normal development of the mechanisms of respiratory control, including ventilatory chemosensitivity.Several studies have questioned whether the ventilatory responses to hypoxia or hypercapnia reflect a genetically controlled and fixed program or are a phenotypic trait that can be modified through experiences, a phenomenon often referred to as developmental plasticity (18; see Ref. 7 for review). For example, studies on ...

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Section: Discussionsupporting

confidence: 61%

Section: Discussionsupporting

confidence: 55%

Section: Discussionmentioning

confidence: 97%

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Ventilatory chemosensitivity of the 1-day-old chicken hatchling after embryonic hypoxia

Szdzuy

Mortola²

2007

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Both embryonic growth and development are adversely affected by prolonged periods of hypoxia (Crossley and Altimiras, 2005;Azzam et al, 2007;Roussel, 2007). Chronic hypoxia negatively affects hatching success (Taylor et al, 1971) as well as post-hatching fitness-related variables including predator avoidance (Roussel, 2007), sexual development (Shang et al, 2006) and development of an unfavorable sex ratio (Shang et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

“…Chronic hypoxia has been shown to decrease embryonic growth rate (Warburton et al, 1995;Crossley and Altimiras, 2005;Roussel, 2007), reduce hatchling mass (Crossley and Altimiras, 2005), delay the development of thermogenesis (Azzam et al, 2007), and reduce predator avoidance ability of juveniles (Roussel, 2007). Moreover, acute hypoxia can have immediate effects on embryos, including reduced metabolic rate (Kam, 1993a;Kam, 1993b) and increased cell death (Devoto, 2006).…”

Section: Introductionmentioning

confidence: 99%

Alternating egg-brooding behaviors create and modulate a hypoxic developmental micro-environment in Children's pythons (Antaresia childreni)

Stahlschmidt

DeNardo

2008

Journal of Experimental Biology

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SUMMARYParental care is a widespread and ecologically relevant adaptation known to enhance the developmental environment of offspring. Parental behaviors, however, may entail both costs and benefits for developing offspring. In Children's pythons (Antaresia childreni), we monitored both maternal egg-brooding behavior and intra-clutch oxygen partial pressure (P O 2) in realtime to assess the effects of various brooding behaviors on P O 2 in the clutch micro-environment at three stages of development. Furthermore, at the same developmental stages, we measured O 2 consumption rates (V O 2) of eggs at varying P O 2 to determine their critical oxygen tension (i.e. the minimal P O 2 that supports normal respiratory gas exchange) and to predict the impact that naturally brooded intra-clutch P O 2 has on embryonic metabolism. At all three stages of development, a tightly coiled brooding posture created an intra-clutch P O 2 that was significantly lower than the surrounding nest environment. Maternal postural adjustments alleviated this hypoxia, and the magnitude of such corrections increased with developmental stage. Mean intraclutch P O 2 decreased with stage of development, probably because of increasing egg V O 2. Additionally, embryo critical oxygen tension increased with developmental stage. Together, these results suggest that python embryos are unable to maintain normal metabolism under brooded conditions during the final 10% of incubation. These results demonstrate that specific parental behaviors can impose obligatory costs to developing offspring and that balancing these behaviors can mediate deleterious consequences.

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Chick embryos have the same pattern of hypoxic lower‐brain activation as fetal mammals

Landry

Hawkins

Lee

et al. 2015

Developmental Neurobiology

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cFos expression (indicating a particular kind of neuronal activation) was examined in embryonic day (E) 18 chick embryos after exposure to 4 h of either normoxia (21% O2), modest hypoxia (15% O2), or medium hypoxia (10% O2). Eight regions of the brainstem and hypothalamus were surveyed, including seven previously shown to respond to hypoxia in late-gestation mammalian fetuses (Breen et al., 1997; Nitsos and Walker, 1999b). Hypoxia-related changes in chick embryo brain activation mirrored those found in fetal mammals with the exception of the medullary Raphe, which showed decreased hypoxic activation, compared with no change in mammals. This difference may be explained by the greater anapyrexic responses of chick embryos relative to mammalian fetuses. Activation in the A1/C1 region was examined in more detail to ascertain whether an O2-sensitive subpopulation of these cells containing heme oxygenase 2 (HMOX2) may drive hypoxic brain responses before the maturation of peripheral O2-sensing. HMOX2-positive and -negative catecholaminergic cells and interdigitating noncatecholaminergic HMOX2-positive cells all showed significant changes in cFos expression to hypoxia, with larger population responses seen in the catecholaminergic cells. Hypoxia-induced activation of lower-brain regions studied here was significantly better correlated with activation of the nucleus of the solitary tract (NTS) than with that of HMOX2-containing A1/C1 neurons. Together, these observations suggest that (1) the functional circuitry controlling prenatal brain responses to hypoxia is strongly conserved between birds and mammals, and (2) NTS neurons are a more dominant driving force for prenatal hypoxic cFos brain responses than O2-sensing A1/C1 neurons.

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Hypoxic incubation blunts the development of thermogenesis in chicken embryos and hatchlings

Cited by 29 publications

References 39 publications

Ventilatory chemosensitivity of the 1-day-old chicken hatchling after embryonic hypoxia

Ventilatory chemosensitivity of the 1-day-old chicken hatchling after embryonic hypoxia

Alternating egg-brooding behaviors create and modulate a hypoxic developmental micro-environment in Children's pythons (Antaresia childreni)

Chick embryos have the same pattern of hypoxic lower‐brain activation as fetal mammals

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