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Hypothalamus‐Pituitary‐Thyroid Axis

Tania M. Ortiga‐Carvalho, Maria I. Chiamolera, Carmen C. Pazos‐Moura, Fredric E. Wondisford

10.1002/cphy.c150027

Source: Volume 6, Issue 3, July 2016

Published online: June 2016

Full Article on Wiley Online Library



ABSTRACT

The hypothalamus‐pituitary‐thyroid (HPT) axis determines the set point of thyroid hormone (TH) production. Hypothalamic thyrotropin‐releasing hormone (TRH) stimulates the synthesis and secretion of pituitary thyrotropin (thyroid‐stimulating hormone, TSH), which acts at the thyroid to stimulate all steps of TH biosynthesis and secretion. The THs thyroxine (T4) and triiodothyronine (T3) control the secretion of TRH and TSH by negative feedback to maintain physiological levels of the main hormones of the HPT axis. Reduction of circulating TH levels due to primary thyroid failure results in increased TRH and TSH production, whereas the opposite occurs when circulating THs are in excess. Other neural, humoral, and local factors modulate the HPT axis and, in specific situations, determine alterations in the physiological function of the axis. The roles of THs are vital to nervous system development, linear growth, energetic metabolism, and thermogenesis. THs also regulate the hepatic metabolism of nutrients, fluid balance and the cardiovascular system. In cells, TH actions are mediated mainly by nuclear TH receptors (210), which modify gene expression. T3 is the preferred ligand of THR, whereas T4, the serum concentration of which is 100‐fold higher than that of T3, undergoes extra‐thyroidal conversion to T3. This conversion is catalyzed by 5′‐deiodinases (D1 and D2), which are TH‐activating enzymes. T4 can also be inactivated by conversion to reverse T3, which has very low affinity for THR, by 5‐deiodinase (D3). The regulation of deiodinases, particularly D2, and TH transporters at the cell membrane control T3 availability, which is fundamental for TH action. © 2016 American Physiological Society. Compr Physiol 6:1387‐1428, 2016.

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Figure 1. Figure 1. Schematic representation of TRH neuron distribution and axonal projections in the median eminence. TRH neurons in the PVN of the mediobasal hypothalamus receive regulatory inputs from other neurons, shown here in the ARC neurons. PVN neurons send axonal projections to the median eminence, where TRH is released and enters into the capillaries of the pituitary‐portal circulation to reach the pituitary. Tanycytes, specialized glial cells that play a role in HPT axis regulation, are shown in the floor of the third ventricle. Tanycytes are part of the ependymal layer (ependimary cells can also be seen in the compound image), and as can be seen in the figure, they have long processes that extend to the median eminence. ARC, arcuate nucleus; PVN, paraventricular nucleus; 3V, third ventricle.
Figure 2. Figure 2. Organization of the mouse TRH gene promoter and translated regions, and a schematic of the posttranslational processing of pre‐pro‐TRH. The TRH gene is represented in the first part of the figure with three regulatory elements in the promoter region (GRE, CRE2, and TRE/Site 4) and three exons (E1, E2, and E3). The pre‐pro‐TRH mRNA is synthetized in the rough endoplasmatic reticulum, and then pre‐pro‐TRH is cleaved to form pro‐TRH in the endoplasmatic reticulum. In the Golgi, pro‐TRH is processed by PC 1/3 to generate smaller intermediate forms, which are then processed in the secretory granules where basic residues (lysine and arginine) are cleaved by PC and removed by carboxy‐peptidases E and D, and the glycine is converted to amide by peptidylglycine alpha‐amidating monooxygenase enzyme, resulting in biologically active TRH. TRH can be inactivated by PPII. GRE, glucocorticoid response element; CRE2, cAMP response element 2; TRE, thyroid hormone response element; PC1/3 and 2, prohormone convertases 1/3 and 2, CPE and CPD, carboxy‐peptidases E and D; PAM, peptidylglycine alpha‐amidating monooxygenase enzyme; PPII, pyroglutamyl peptidase II.
Figure 3. Figure 3. Schematic figure showing the main inputs to TRH neurons from the ARC, the DMN, and the medulla, as well as integration with leptin signaling from adipose tissue. TRH neurons in the PVN receive stimulatory and inhibitory inputs from several different neuron types in the ARC, the DMN, and medulla as it is represented in the figure by black arrows and red lines, respectively. Adipose tissue secretes leptin and other regulatory signals to both the ARC and DMN, as well as directly to TRH neurons in the PVN. PVN, paraventricular nucleus; ARC, arcuate nucleus; DMN, dorsomedial nucleus; 3V, third ventricle; AgRP, agouti‐related protein; NPY, neuropeptide Y; αMSH, melanocortin stimulating hormone; CART, cocaine and amphetamine‐regulated transcript.
Figure 4. Figure 4. Adeno‐pituitary development. Temporal and spatial activation of pituitary transcription factors. Solid arrows indicate the activation of expression, dotted arrows indicate an unknown role in the activation of expression, dashed arrows indicate an undefined role and dashdot arrows indicate an action of an important factor in the maintenance of long‐term cell function. BMP2, bone morphogenic protein 2; EGR1, early growth response 1; ER, oestrogen receptor; FGF8, fibroblast growth factor 8; GATA2, GATA‐binding protein 2; HESX1, HESX homeobox 1; ISL1, ISL LIM homeobox 1; LHX3, LIM homeobox 3; LHX4, LIM homeobox 4; LIF, leukaemia inhibitory factor; MSX1, msh homeobox 1; NeuroD1, neurogenic differentiation 1; PIT1, POU class 1 homeobox 1; PITX1, paired‐like homeodomain 1; PITX2, paired‐like homeodomain 2; POMC, pro‐opiomelanocortin; PROP1, prophet of Pit‐1; RAR, retinoic acid receptor; SF1, steroidogenic factor 1; T3r, thyroid hormone nuclear receptor; TEF, thyrotrope embryonic factor; TPIT, T‐box 19; Zn15, zinc finger protein Zn15. Used with permission, from figure 2 of 123.
Figure 5. Figure 5. N‐linked oligosacharides of thyrotrophin. The sulfated biantennary structure (A) representes that of bovine TSH and bovine luteinizing hormone (LH). The sulfated and sialylated oligosaccharide is typical of human TSH (hTSH) and human LH. The sialylated nonsulfated structure (C) representes that of recombinant hTSH expressed in Chinese hamster ovary cells. Mannose (o), N‐acetyl‐glucosamine (quadrado preto), N‐acetyl‐galactosamine (circulo preto), fucose (triangulo preto), galactose (Δ), and sialic acid (NeuAc). Used with permission, from figure 4 of 516.
Figure 6. Figure 6. Regulation of the HPT axis. The PVN in the hypothalamus releases TRH, which acts on pituitary thyrotropes to stimulate TSH synthesis. TSH acts on thyrocytes to stimulate all steps of thyroid hormone synthesis. The thyroid hormones T4 and T3 act on PVN neurons and on the thyrotropes to inhibit TRH and TSH synthesis and release and this feedback regulation is the main regulatory mechanism of thyroid function. The pituitary thyrotropes are also regulated by local factors in through autocrine and paracrine pathways. Green arrows represent stimulation, and red arrows represent inhibition.
Figure 7. Figure 7. TSH Circadian Rhythm in normal men and women. Twenty‐four‐hour serum TSH concentration time series in 24 healthy men and 22 healthy women. Blood samples were taken every 10 min for 24 h. Blood sampling started at 09:00h. Lights were off between 23:00 h until 07:30 h next morning. Data are shown as the group mean and SEM. Republished with permission of Endocrine Society, from figure 1 of 454.
Figure 8. Figure 8. Thyroid differentiation factors. Factors are represented by ovals; gene promoters are represented by retangles. Binding of a regulator to a promoter is indicated by a solid arrow. Genes encoding regulators are linked to their respective regulators by dashed arrows. Physical interaction between factors is indicated by a thick line arrow. Republished with permission of Endocrine Society, from figure 2 of 121.
Figure 9. Figure 9. Representation of a follicular thyroid cell showing the main steps of thyroid hormone synthesis. A follicular thyroid cell is shown. In the basal membrane, circulating iodine actively enters the cell using the sodium gradient through NIS; the transport of iodide from the cytosol to the colloid occurs via another protein, PDS. In the colloid, iodide oxidation, organification of thyroglobulin forming MIT and DIT, and coupling of MIT and DIT resulting in T3 and T4 are mediated by TPO, an enzyme located in the apical membrane that utilizes H2O2 generated by DUOX2 (also located in the apical membrane) to mediate its enzymatic effects. Colloid containing thyroglobulin, thyroid hormones, MIT and DIT are incorporated by the cell into vesicles containing proteolytic enzymes, which cleave thyroglobulin to generate the free thyroid hormones T3 and T4 as well as MIT and DIT; the remaining iodide is recycled and used again by the cell. Free T3 and T4 are then released into circulation by MCT8. NIS, sodium‐iodide symporter; PDS, Pendrin; DUOX, dual oxidase type 2; TPO, thyroperoxidase; MIT, monoiodothyrosine; DIT, diiodotyrosine; MCT8, monocarboxylate transporter 8.
Figure 10. Figure 10. Thyroid hormone metabolism. Schematic representation of the deiodinase‐mediated activation or inactivation of thyroxine and triiodothyronine. Used with permission of Springer Science+Business Media, figure 1 from 336.
Figure 11. Figure 11. Origin of THR‐bound T3. Created using data from 50, 104, and 496. Total THR occupancy for each rat tissue is represented by percentage of THR saturation. (L)T3 refers to T3 generated from T4. (P)T3 refers to plasma T3.
Figure 12. Figure 12. Subtypes of THRs and tissue distributions. THRα1, THRβ1, THRβ2, and THRβ1 are able to bind T3 and form dimers. The DBD of all THRs subtypes are highly conserved; however, the subtypes THRα2, THRΔα1‐2, and THRΔβ3 are unable to bind T3 due to important changes in the LBD. AF2, activation function 2. See details in the text.
Figure 13. Figure 13. Schematic representation of TRE arrangements. The arrows represent sequences of consensus nucleotides half‐sites: (A) direct repeat orientation, (B) palindrome, and (C) inverted palindrome. TRE, thyroid hormone response element.
Figure 14. Figure 14. Pattern of THR and RXR interactions with corepressors and coactivators. In the absence of T3, a co‐repressor is bound to the RXR‐THR heterodimer at the positive TRE, thereby actively repressing target gene expression. When T3 binds to the THR dimer, the co‐repressor is released and co‐activators are recruited, which results in activation of gene transcription. CoA, co‐activator; CoR, co‐repressor; RXR, retinoid X receptor; THR, thyroid hormone receptor; TER, thyroid‐hormone responsive elemento. Used with permission, from figure 3 of 406.
Figure 15. Figure 15. Thyroid hormone regulation of metabolic pathways. TRH and TSH respond primarily to circulating serum T4, converted in the hypothalamus and pituitary to T3 by the 5′‐deiodinase type 2 (D2). The monocarboxylate transporter 8 (MCT8) is required for T3 transport into the pituitary and hypothalamus. A, parvalbuminergic neurons (PBN): PBN are directly linked to the regulation of cardiovascular function, blood pressure, and body temperature. B, paraventricular nucleus of the hypothlamus (PVN): leptin provides feedback at the PVN, stimulates signal transducer and activator of transcription (STAT)3 phosphorylation (STAT3‐P*), which directly stimulates TRH expression. C, ventromedial nucleus of the hypothalamus (VMH): hyperthyroidism or T3 treatment stimulates de novo fatty acid synthesis in the VMH, which inhibits AMPK phosphorylation and increases fatty acid synthase (FAS) activity. Increased hypothalamic lipid synthesis is associated with activation of the sympathetic nervous system (SNS) which stimulates brown adipose tissue (BAT). D, BAT: adrenergic signaling through the β3‐adrenergic receptor (AR) stimulates UCP1 gene expression, stimulates D2 activity by deubiquitination, and promotes thermogenesis and weight loss. The metabolic signal from bile acid via the G protein‐coupled membrane bile acid receptor (TGR5) has been shown in one model to stimulate D2 activity and local T3 production, which further stimulates BAT lipolysis, UCP1 expression, and thermogenesis. E, white adipose tissue (WAT): T3 stimulates local production of norepinephrine (NE), increasing lipolysis and reducing body fat. F, liver: T3 is involved in both cholesterol and fatty acid metabolism. HOMGCR, 3‐hydroxy‐3‐methylglutaryl‐CoA reductase; ACC1, acetyl‐CoA carboxylase 1; CYP7a1, cytochrome P‐450 7A1; CPT‐1α, carnitine palmitoyltransferase 1α; LDL‐R, low‐density lipoprotein receptor. G, muscle: Forkhead box O3 (FoxO3) induces D2 expression, increases local T3 in skeletal muscle, and promotes T3‐target gene expression; myoD, myosin heavy chain (MHC) and sarcoplasmic reticulum Ca2+‐ATPase (SERCA). Local T3 also determines the relative expression level of MHC and SERCA isoforms. T3 stimulates SERCA, which hydrolyzes ATP and increases energy expenditure. H, pancreas: T3 and THR are required for normal pancreatic development and function. In rat pancreatic β cells, expression of THR and D2 are activated during normal development. T3 treatment enhances Mafa (v‐maf musculoaponeurotic fibrosarcoma oncogene homolog A), the key factor for maturation of β cells to secrete insulin in response to glucose. T3 stimulates cyclin D1 (CD1) and promotes proliferation. Used with permission, from figure 1 of 378.
Figure 16. Figure 16. Oxygen consumption (QO2) in hepatocytes from hypo‐, eu‐ and hyperthyroid rats. Non‐Mit, non mitocondrial. Used with permission, from figure 7 of 496.


Figure 1. Schematic representation of TRH neuron distribution and axonal projections in the median eminence. TRH neurons in the PVN of the mediobasal hypothalamus receive regulatory inputs from other neurons, shown here in the ARC neurons. PVN neurons send axonal projections to the median eminence, where TRH is released and enters into the capillaries of the pituitary‐portal circulation to reach the pituitary. Tanycytes, specialized glial cells that play a role in HPT axis regulation, are shown in the floor of the third ventricle. Tanycytes are part of the ependymal layer (ependimary cells can also be seen in the compound image), and as can be seen in the figure, they have long processes that extend to the median eminence. ARC, arcuate nucleus; PVN, paraventricular nucleus; 3V, third ventricle.


Figure 2. Organization of the mouse TRH gene promoter and translated regions, and a schematic of the posttranslational processing of pre‐pro‐TRH. The TRH gene is represented in the first part of the figure with three regulatory elements in the promoter region (GRE, CRE2, and TRE/Site 4) and three exons (E1, E2, and E3). The pre‐pro‐TRH mRNA is synthetized in the rough endoplasmatic reticulum, and then pre‐pro‐TRH is cleaved to form pro‐TRH in the endoplasmatic reticulum. In the Golgi, pro‐TRH is processed by PC 1/3 to generate smaller intermediate forms, which are then processed in the secretory granules where basic residues (lysine and arginine) are cleaved by PC and removed by carboxy‐peptidases E and D, and the glycine is converted to amide by peptidylglycine alpha‐amidating monooxygenase enzyme, resulting in biologically active TRH. TRH can be inactivated by PPII. GRE, glucocorticoid response element; CRE2, cAMP response element 2; TRE, thyroid hormone response element; PC1/3 and 2, prohormone convertases 1/3 and 2, CPE and CPD, carboxy‐peptidases E and D; PAM, peptidylglycine alpha‐amidating monooxygenase enzyme; PPII, pyroglutamyl peptidase II.


Figure 3. Schematic figure showing the main inputs to TRH neurons from the ARC, the DMN, and the medulla, as well as integration with leptin signaling from adipose tissue. TRH neurons in the PVN receive stimulatory and inhibitory inputs from several different neuron types in the ARC, the DMN, and medulla as it is represented in the figure by black arrows and red lines, respectively. Adipose tissue secretes leptin and other regulatory signals to both the ARC and DMN, as well as directly to TRH neurons in the PVN. PVN, paraventricular nucleus; ARC, arcuate nucleus; DMN, dorsomedial nucleus; 3V, third ventricle; AgRP, agouti‐related protein; NPY, neuropeptide Y; αMSH, melanocortin stimulating hormone; CART, cocaine and amphetamine‐regulated transcript.


Figure 4. Adeno‐pituitary development. Temporal and spatial activation of pituitary transcription factors. Solid arrows indicate the activation of expression, dotted arrows indicate an unknown role in the activation of expression, dashed arrows indicate an undefined role and dashdot arrows indicate an action of an important factor in the maintenance of long‐term cell function. BMP2, bone morphogenic protein 2; EGR1, early growth response 1; ER, oestrogen receptor; FGF8, fibroblast growth factor 8; GATA2, GATA‐binding protein 2; HESX1, HESX homeobox 1; ISL1, ISL LIM homeobox 1; LHX3, LIM homeobox 3; LHX4, LIM homeobox 4; LIF, leukaemia inhibitory factor; MSX1, msh homeobox 1; NeuroD1, neurogenic differentiation 1; PIT1, POU class 1 homeobox 1; PITX1, paired‐like homeodomain 1; PITX2, paired‐like homeodomain 2; POMC, pro‐opiomelanocortin; PROP1, prophet of Pit‐1; RAR, retinoic acid receptor; SF1, steroidogenic factor 1; T3r, thyroid hormone nuclear receptor; TEF, thyrotrope embryonic factor; TPIT, T‐box 19; Zn15, zinc finger protein Zn15. Used with permission, from figure 2 of 123.


Figure 5. N‐linked oligosacharides of thyrotrophin. The sulfated biantennary structure (A) representes that of bovine TSH and bovine luteinizing hormone (LH). The sulfated and sialylated oligosaccharide is typical of human TSH (hTSH) and human LH. The sialylated nonsulfated structure (C) representes that of recombinant hTSH expressed in Chinese hamster ovary cells. Mannose (o), N‐acetyl‐glucosamine (quadrado preto), N‐acetyl‐galactosamine (circulo preto), fucose (triangulo preto), galactose (Δ), and sialic acid (NeuAc). Used with permission, from figure 4 of 516.


Figure 6. Regulation of the HPT axis. The PVN in the hypothalamus releases TRH, which acts on pituitary thyrotropes to stimulate TSH synthesis. TSH acts on thyrocytes to stimulate all steps of thyroid hormone synthesis. The thyroid hormones T4 and T3 act on PVN neurons and on the thyrotropes to inhibit TRH and TSH synthesis and release and this feedback regulation is the main regulatory mechanism of thyroid function. The pituitary thyrotropes are also regulated by local factors in through autocrine and paracrine pathways. Green arrows represent stimulation, and red arrows represent inhibition.


Figure 7. TSH Circadian Rhythm in normal men and women. Twenty‐four‐hour serum TSH concentration time series in 24 healthy men and 22 healthy women. Blood samples were taken every 10 min for 24 h. Blood sampling started at 09:00h. Lights were off between 23:00 h until 07:30 h next morning. Data are shown as the group mean and SEM. Republished with permission of Endocrine Society, from figure 1 of 454.


Figure 8. Thyroid differentiation factors. Factors are represented by ovals; gene promoters are represented by retangles. Binding of a regulator to a promoter is indicated by a solid arrow. Genes encoding regulators are linked to their respective regulators by dashed arrows. Physical interaction between factors is indicated by a thick line arrow. Republished with permission of Endocrine Society, from figure 2 of 121.


Figure 9. Representation of a follicular thyroid cell showing the main steps of thyroid hormone synthesis. A follicular thyroid cell is shown. In the basal membrane, circulating iodine actively enters the cell using the sodium gradient through NIS; the transport of iodide from the cytosol to the colloid occurs via another protein, PDS. In the colloid, iodide oxidation, organification of thyroglobulin forming MIT and DIT, and coupling of MIT and DIT resulting in T3 and T4 are mediated by TPO, an enzyme located in the apical membrane that utilizes H2O2 generated by DUOX2 (also located in the apical membrane) to mediate its enzymatic effects. Colloid containing thyroglobulin, thyroid hormones, MIT and DIT are incorporated by the cell into vesicles containing proteolytic enzymes, which cleave thyroglobulin to generate the free thyroid hormones T3 and T4 as well as MIT and DIT; the remaining iodide is recycled and used again by the cell. Free T3 and T4 are then released into circulation by MCT8. NIS, sodium‐iodide symporter; PDS, Pendrin; DUOX, dual oxidase type 2; TPO, thyroperoxidase; MIT, monoiodothyrosine; DIT, diiodotyrosine; MCT8, monocarboxylate transporter 8.


Figure 10. Thyroid hormone metabolism. Schematic representation of the deiodinase‐mediated activation or inactivation of thyroxine and triiodothyronine. Used with permission of Springer Science+Business Media, figure 1 from 336.


Figure 11. Origin of THR‐bound T3. Created using data from 50, 104, and 496. Total THR occupancy for each rat tissue is represented by percentage of THR saturation. (L)T3 refers to T3 generated from T4. (P)T3 refers to plasma T3.


Figure 12. Subtypes of THRs and tissue distributions. THRα1, THRβ1, THRβ2, and THRβ1 are able to bind T3 and form dimers. The DBD of all THRs subtypes are highly conserved; however, the subtypes THRα2, THRΔα1‐2, and THRΔβ3 are unable to bind T3 due to important changes in the LBD. AF2, activation function 2. See details in the text.


Figure 13. Schematic representation of TRE arrangements. The arrows represent sequences of consensus nucleotides half‐sites: (A) direct repeat orientation, (B) palindrome, and (C) inverted palindrome. TRE, thyroid hormone response element.


Figure 14. Pattern of THR and RXR interactions with corepressors and coactivators. In the absence of T3, a co‐repressor is bound to the RXR‐THR heterodimer at the positive TRE, thereby actively repressing target gene expression. When T3 binds to the THR dimer, the co‐repressor is released and co‐activators are recruited, which results in activation of gene transcription. CoA, co‐activator; CoR, co‐repressor; RXR, retinoid X receptor; THR, thyroid hormone receptor; TER, thyroid‐hormone responsive elemento. Used with permission, from figure 3 of 406.


Figure 15. Thyroid hormone regulation of metabolic pathways. TRH and TSH respond primarily to circulating serum T4, converted in the hypothalamus and pituitary to T3 by the 5′‐deiodinase type 2 (D2). The monocarboxylate transporter 8 (MCT8) is required for T3 transport into the pituitary and hypothalamus. A, parvalbuminergic neurons (PBN): PBN are directly linked to the regulation of cardiovascular function, blood pressure, and body temperature. B, paraventricular nucleus of the hypothlamus (PVN): leptin provides feedback at the PVN, stimulates signal transducer and activator of transcription (STAT)3 phosphorylation (STAT3‐P*), which directly stimulates TRH expression. C, ventromedial nucleus of the hypothalamus (VMH): hyperthyroidism or T3 treatment stimulates de novo fatty acid synthesis in the VMH, which inhibits AMPK phosphorylation and increases fatty acid synthase (FAS) activity. Increased hypothalamic lipid synthesis is associated with activation of the sympathetic nervous system (SNS) which stimulates brown adipose tissue (BAT). D, BAT: adrenergic signaling through the β3‐adrenergic receptor (AR) stimulates UCP1 gene expression, stimulates D2 activity by deubiquitination, and promotes thermogenesis and weight loss. The metabolic signal from bile acid via the G protein‐coupled membrane bile acid receptor (TGR5) has been shown in one model to stimulate D2 activity and local T3 production, which further stimulates BAT lipolysis, UCP1 expression, and thermogenesis. E, white adipose tissue (WAT): T3 stimulates local production of norepinephrine (NE), increasing lipolysis and reducing body fat. F, liver: T3 is involved in both cholesterol and fatty acid metabolism. HOMGCR, 3‐hydroxy‐3‐methylglutaryl‐CoA reductase; ACC1, acetyl‐CoA carboxylase 1; CYP7a1, cytochrome P‐450 7A1; CPT‐1α, carnitine palmitoyltransferase 1α; LDL‐R, low‐density lipoprotein receptor. G, muscle: Forkhead box O3 (FoxO3) induces D2 expression, increases local T3 in skeletal muscle, and promotes T3‐target gene expression; myoD, myosin heavy chain (MHC) and sarcoplasmic reticulum Ca2+‐ATPase (SERCA). Local T3 also determines the relative expression level of MHC and SERCA isoforms. T3 stimulates SERCA, which hydrolyzes ATP and increases energy expenditure. H, pancreas: T3 and THR are required for normal pancreatic development and function. In rat pancreatic β cells, expression of THR and D2 are activated during normal development. T3 treatment enhances Mafa (v‐maf musculoaponeurotic fibrosarcoma oncogene homolog A), the key factor for maturation of β cells to secrete insulin in response to glucose. T3 stimulates cyclin D1 (CD1) and promotes proliferation. Used with permission, from figure 1 of 378.


Figure 16. Oxygen consumption (QO2) in hepatocytes from hypo‐, eu‐ and hyperthyroid rats. Non‐Mit, non mitocondrial. Used with permission, from figure 7 of 496.
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Article Title: Hypothalamus‐Pituitary‐Thyroid Axis
 

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Tania M. Ortiga‐Carvalho, Maria I. Chiamolera, Carmen C. Pazos‐Moura, Fredric E. Wondisford. Hypothalamus‐Pituitary‐Thyroid Axis. Compr Physiol 2016, 6: 1387-1428. doi: 10.1002/cphy.c150027