Andre Seale | University of Hawaii at Manoa (original) (raw)

Papers by Andre Seale

The almost limitless complexity of biology has led to two general approaches to understanding bio... more The almost limitless complexity of biology has led to two general approaches to understanding biological phenomena. One approach is dominated by reductionism in which high-level phenomena of whole systems are viewed as emerging from relatively simple and generally understood interactions at a substantially lower level. Although this approach is theoretically general, it can become intractable in practice when attempting to simultaneously explain a wide range of systems. A second approach is for specialists to investigate biological phenomena within one of many different hierarchical levels of description that are separated to decouple from concerns at other levels. Although this approach reduces the explanatory burden on specialists that operate within each level, it also reduces integration from insights gained at other levels. Thus, as beneficial as these approaches have been, they limit the scope and integration of knowledge across scales of biological organization to the detriment of a truly synoptic view of life. The challenge is to find a theoretical and experimental framework that facilitates a broader understanding of the hierarchy of life-providing permeability for the exchange of ideas among disciplinary specialists without discounting the peculiarities that have come to define those disciplines. For this purpose, coarse-grained, scale-invariant properties, and resources need to be identified that describe the characteristic features of a living system at all spatiotemporal scales. The approach will be aided by a common vernacular that underscores the realities of biological connections across a wide range of scales. Therefore, in this vision paper, we propose a conceptual approach based on four identified resources-energy, conductance, storage, and information (ECSI)-to reintegrate biological studies with the aim of unifying life sciences under resource limitations. We argue that no functional description of a living system is complete without accounting for at least all four of these resources. Thus, making these resources explicit will help to identify commonalities to aid in transdisciplinary discourse as well as opportunities for integrating among the differently scoped areas of specialized inquiry. The proposed conceptual framework for living systems should be valid across all scales and may uncover potential limitations of existing hypotheses and help researchers develop new hypotheses addressing fundamental processes of life without having to resort to reductionism.

Frontiers in Aging, 2021

Euryhaline teleost fish are characterized by their ability to tolerate a wide range of environmen... more Euryhaline teleost fish are characterized by their ability to tolerate a wide range of environmental salinities by modifying the function of osmoregulatory cells and tissues. In this study, we experimentally addressed the age-related decline in the sensitivity of osmoregulatory transcripts associated with a transfer from fresh water (FW) to seawater (SW) in the euryhaline teleost, Mozambique tilapia, Oreochromis mossambicus. The survival rates of tilapia transferred from FW to SW were inversely related with age, indicating that older fish require a longer acclimation period during a salinity challenge. The relative expression of Na+/K+/2Cl− cotransporter 1a (nkcc1a), which plays an important role in hyposmoregulation, was significantly upregulated in younger fish after SW transfer, indicating a clear effect of age in the sensitivity of branchial ionocytes. Prolactin (Prl), a hyperosmoregulatory hormone in O. mossambicus, is released in direct response to a fall in extracellular osmolality. Prl cells of 4-month-old tilapia were sensitive to hyposmotic stimuli, while those of >24-month-old fish did not respond. Moreover, the responsiveness of branchial ionocytes to Prl was more robust in younger fish. Taken together, multiple aspects of osmotic homeostasis, from osmoreception to hormonal and environmental control of osmoregulation, declined in older fish. This decline appears to undermine the ability of older fish to survive transfer to hyperosmotic environments.

General and Comparative Endocrinology, 2022

Across the vertebrate lineage, sexual dimorphism in body size is a common phenomenon that results... more Across the vertebrate lineage, sexual dimorphism in body size is a common phenomenon that results from tradeoffs between growth and reproduction. To address how key hormones that regulate growth and reproduction interact in teleost fishes, we studied Mozambique tilapia (Oreochromis mossambicus) to determine whether the activities of luteinizing hormone (Lh) are modulated by growth hormone (Gh), and conversely, whether targets of Gh are affected by the presence of Lh. In particular, we examined how gonadal morphology and specific gene transcripts responded to ovine GH (oGH) and/or LH (oLH) in hypophysectomized male and female tilapia. Hypophysectomized females exhibited a diminished gonadosomatic index (GSI) concomitant with ovarian follicular atresia. The combination of oGH and oLH restored GSI and ovarian morphology to conditions observed in sham-operated controls. A similar pattern was observed for GSI in males. In control fish, gonadal gh receptor (ghr2) and estrogen receptor β (erβ) expression was higher in females versus males. A combination of oGH and oLH restored erβ and arβ in females. In males, testicular insulin-like growth factor 3 (igf3) expression was reduced following hypophysectomy and subsequently restored to control levels by either oGH or oLH. By contrast, the combination of both hormones was required to recover ovarian igf3 expression in females. In muscle, ghr2 expression was more responsive to oGH in males versus females. In the liver of hypophysectomized males, igf2 expression was diminished by both oGH and oLH; there was no effect of hypophysectomy, oGH, or oLH on igf2 expression in females. Collectively, our results indicate that gene transcripts associated with growth and reproduction exhibit sex-specific responses to oGH and oLH. These responses reflect, at least in part, how hormones mediate trade-offs between growth and reproduction, and thus sexual dimorphism, in teleost fishes.

General and Comparative Endocrinology, 2023

In estuarine environments, euryhaline fish maintain a narrow range of internal osmolality despite... more In estuarine environments, euryhaline fish maintain a narrow range of internal osmolality despite daily changes in environmental salinity that can range from fresh water (FW) to seawater (SW). The capacity of euryhaline fish to maintain homeostasis in a range of environmental salinities is primarily facilitated by the neuroendocrine system. One such system, the hypothalamic-pituitary-interrenal (HPI) axis, culminates in the release of corticosteroids such as cortisol into circulation. Cortisol functions as both a mineralocorticoid and glucocorticoid in fish because of its roles in osmoregulation and metabolism, respectively. The gill, a key site for osmoregulation, and the liver, the primary storage site for glucose, are known targets of cortisol's actions during salinity stress. While cortisol facilitates acclimation to SW environments, less is known on its role during FW adaptation. In this study, we characterized the responses of plasma cortisol, mRNA expression of pituitary pro-opiomelanocortin (pomc), and mRNA expression of liver and gill corticosteroid receptors (gr1, gr2, and mr) in the euryhaline Mozambique tilapia (Oreochromis mossambicus) under salinity challenges. Specifically, tilapia were subjected to salinity transfer regimes from steady-state FW to SW, SW to FW (experiment 1) or steady state FW or SW to tidal regimen (TR, experiment 2). In experiment 1, fish were sampled at 0 h, 6 h, 1, 2, and 7 d post transfer; while in experiment 2, fish were sampled at day 0 and day 15. We found a rise in pituitary pomc expression and plasma cortisol following transfer to SW while branchial corticosteroid receptors were immediately downregulated after transfer to FW. Moreover, branchial expression of corticosteroid receptors changed with each salinity phase of the TR, suggesting rapid environmental modulation of corticosteorid action. Together, these results support the role of the HPI-axis in promoting salinity acclimation, including in dynamically-changing environments.

Comparative Biochemistry and Physiology, 2022

In euryhaline fish, prolactin (Prl) plays a key role in freshwater acclimation. Prl release in th... more In euryhaline fish, prolactin (Prl) plays a key role in freshwater acclimation. Prl release in the rostral pars distalis (RPD) of the pituitary is directly stimulated by a fall in extracellular osmolality. Recently, we identified several putative transcription factor modules (TFM) predicted to bind to the promoter regions of the two prl isoforms in Mozambique tilapia, Oreochromis mossambicus. We characterized the effects of extracellular osmolality on the activation of these TFMs from RPDs, in vivo and in vitro. OCT1_PIT1 01, CEBP_CEBP 01 and BRNF_RXRF 01 were significantly activated in freshwater (FW)-acclimated tilapia RPDs while SORY_PAX3 02 and SP1F_SP1F 06, SP1F_SP1F 09 were significantly activated in seawater (SW)-counterparts. Short-term incubation of SW-acclimated tilapia RPDs in hyposmotic media (280 mOsm/kg) resulted in activation of CAAT_AP1F 01, OCT1_CEBP 01, AP1F_SMAD 01, GATA_SP1F 01, SORY_PAX6 01 and CREB_EBOX 02, EBOX_AP2F 01, EBOX_MITF 01 while hyperosmotic media (420 mOsm/kg) activated SORY_PAX3 02 and AP1F_SMAD 01 in FW-tilapia. Short-term incubation of dispersed Prl cells from FW-acclimated fish exposed to hyperosmotic conditions decreased pou1f1, pou2f1b, stat3, stat1a and ap1b1 expression, while pou1f1, pou2f1b, and stat3 were inversely related to osmolality in their SW-counterparts. Further, in Prl cells of SW-tilapia, creb3l1 was suppressed in hyposmotic media. Collectively, our results indicate that multiple TFMs are involved in regulating prl transcription at different acclimation salinities and, together, they modulate responses of Prl cells to changes in extracellular osmolality. These responses reflect the complexity of osmosensitive molecular regulation of the osmoreceptive Prl cell of a euryhaline teleost.

American Journal of Physiology, 2022

Prolactin (PRL) cells within the rostral pars distalis (RPD) of euryhaline and eurythermal Mozamb... more Prolactin (PRL) cells within the rostral pars distalis (RPD) of euryhaline and eurythermal Mozambique tilapia, Oreochromis mossambicus,
rapidly respond to a hyposmotic stimulus by releasing two distinct PRL isoforms, PRL188 and PRL177. Here, we describe
how environmentally relevant temperature changes affected mRNA levels of prl188 and prl177 and the release of immunoreactive
prolactins from RPDs and dispersed PRL cells. When applied under isosmotic conditions (330 mosmol/kgH2O), a 6 C rise in temperature
stimulated the release of PRL188 and PRL177 from both RPDs and dispersed PRL cells under perifusion. When exposed
to this same change in temperature, 50% of dispersed PRL cells gradually increased in volume by 8%, a response partially
inhibited by the water channel blocker, mercuric chloride. Following their response to increased temperature, PRL cells remained
responsive to a hyposmotic stimulus (280 mosmol/kgH2O). The mRNA expression of transient potential vanilloid 4, a Ca2þ-channel
involved in hyposmotically induced PRL release, was elevated in response to a rise in temperature in dispersed PRL cells
and RPDs at 6 and 24 h, respectively; prl188 and prl177 mRNAs were unaffected. Our findings indicate that thermosensitive PRL
release is mediated, at least partially, through a cell-volume-dependent pathway similar to how osmoreceptive PRL release is
achieved.

General and Comparative Endocrinology, 2002

In the tilapia (Oreochromis mossambicus), as in many teleosts, prolactin (PRL) plays a major role... more In the tilapia (Oreochromis mossambicus), as in many teleosts, prolactin (PRL) plays a major role in osmoregulation in freshwater. Recently, PRL-releasing peptides (PrRPs) have been characterized in mammals. Independently, a novel C-terminal RF (arginine-phenylalanine) amide peptide (Carrasius RF amide; C-RFa), which is structurally related to mammalian PrRPs, has been isolated from the brain of the Japanese crucian carp. The putative PrRP was purified from an acid extract of tilapia brain by affinity chromatography with antibody against synthetic C-RFa and HPLC on a reverse-phase ODS-120 column. The tilapia PrRP cDNA was subsequently cloned by polymerase chain reaction. The cDNA consists of 619 bp encoding a preprohormone of 117 amino acids. Sequence comparison of the isolated peptide and the preprohormone revealed that tilapia PrRP contains 20 amino acids and is identical to C-RFa. Incubation of the tilapia pituitary with synthetic C-RFa (100 nM) significantly stimulated the release of two forms of tilapia PRL (PRL 188 and PRL 177 ). However, the effect of C-RFa was less pronounced than the marked increase in PRL release in response to hyposmotic medium. The ability of C-RFa to stimulate PRL release appears to be specific, since C-RFa failed to stimulate growth hormone release from the pituitary in organ culture. In contrast, rat and human PrRPs had no effect on PRL release. C-RFa was equipotent with chicken GnRH in stimulating PRL release in the pituitary preincubated with estradiol 17␤. Circulating levels of PRL were significantly increased 1 h after intraperitoneal injection of 0.1 g/g of C-RFa in female tilapia in freshwater but not in males. These results suggest that C-RFa is physiologically involved in the control of PRL secretion in tilapia. © 2002 Elsevier Science (USA)

General and Comparative Endocrinology, 2002

Prolactin (PRL) plays a central role in freshwater (FW) adaptation in teleost fish. Evidence now ... more Prolactin (PRL) plays a central role in freshwater (FW) adaptation in teleost fish. Evidence now suggests that growth hormone (GH) acts in the seawater (SW) adaptation in at least some euryhaline fish. Reflecting its important role in FW adaptation, plasma levels of PRL 188 and PRL 177 are higher in tilapia (Oreochromis mossambicus) adapted to FW than in those adapted to SW. A transient but significant increase in plasma GH was observed 6 h after transfer from FW to SW. Elevated plasma PRL levels were seen in association with reductions in plasma osmolality after blood withdrawal in FW fish whereas no significant change was seen in plasma GH levels. When pituitaries from FW tilapia were incubated for 7 days, secretion of both PRLs was significantly greater in hyposmotic medium than in hyperosmotic medium for the first 24 h. Secretion of GH from the same pituitary was relatively low during this period compared with PRL secretion. No consistent effect of medium osmolality on GH release was seen for the first day, but its cumulative release was increased significantly in hyperosmotic medium after 2 days and thereafter. On the other hand, ACTH release was extremely low compared with the secretion of PRLs and GH and there was no consistent effect of medium osmolality. These results indicate that PRL release from the tilapia pituitary is stimulated both in vivo and in vitro as extracellular osmolality is reduced, whereas the secretion of GH increases temporarily when osmolality is increased. ACTH seems to be relatively insensitive to the changes in environmental osmolality.

Cellular Physiology and Biochemistry, 2002

Prolactin (PRL) cells from the euryhaline tilapia, Oreochromis mossambicus, behave like osmorecep... more Prolactin (PRL) cells from the euryhaline tilapia, Oreochromis mossambicus, behave like osmoreceptors by responding directly to reductions in medium osmolality with increased secretion of the osmoregulatory hormone PRL. Extracellular Ca 2+ is essential for the transduction of a hyposmotic stimulus into PRL release. In the current study, the presence and possible role of intracellular Ca 2+ stores during hyposmotic stimulation was investigated using pharmacological approaches. Changes in intracellular Ca 2+ concentration were measured with fura-2 in isolated PRL cells. Intracellular Ca 2+ stores were depleted in dispersed PRL cells with thapsigargin (1 µM) or cyclopiazonic acid (CPA, 10 µM). Preincubation with thapsigargin prevented the rise in [Ca 2+ ] i induced by lysophosphatidic acid (LPA, 1 µM), an activator of the IP 3 signalling cascade, but did not prevent the hyposmotically-induced rise in [Ca 2+ ] i in medium with normal [Ca 2+ ] (2mM). Pre-treatment with CPA produced similar results. Prolactin release from dispersed cells followed a pattern that paralleled observed changes in [Ca 2+ ] i . CPA inhibited LPAinduced prolactin release but not hyposmoticallyinduced release. Xestospongin C (1µM), an inhibitor of IP 3 receptors, had no effect on hyposmoticallyinduced PRL release. Pre-exposure to caffeine (10mM) or ryanodine (1µM) did not prevent a hyposmotically-induced rise in [Ca 2+ ] i. Taken together these results indicate the presence of IP 3 and ryanodine-sensitive Ca 2+ stores in tilapia PRL cells. However, the rapid rise in intracellular [Ca 2+ ] needed for acute PRL release in response to hyposmotic medium can occur independently of these intracellular Ca 2+ stores.

American Journal of Physiology, 2003

Cell volume increase and extracellular Ca 2ϩ are needed for hyposmotically induced prolactin rele... more Cell volume increase and extracellular Ca 2ϩ are needed for hyposmotically induced prolactin release in tilapia. tilapia (Oreochromis mossambicus), as in many euryhaline teleost fish, prolactin (PRL) plays a central role in freshwater adaptation, acting on osmoregulatory surfaces to reduce ion and water permeability and increase solute retention. Consistent with these actions, PRL release is stimulated as extracellular osmolality is reduced both in vivo and in vitro. In the current experiments, a perfusion system utilizing dispersed PRL cells was developed for permitting the simultaneous measurement of cell volume and PRL release. Intracellular Ca 2ϩ was monitored using fura 2-loaded cells under the same conditions. When PRL cells were exposed to hyposmotic medium, an increase in PRL cell volume preceded the increase in PRL release. Cell volume increased in proportion to decreases of 15 and 30% in osmolality. However, regulatory volume decrease was clearly seen only after a 30% reduction. The hyposmotically induced PRL release was sharply reduced in Ca 2ϩ -deleted hyposmotic medium, although cell volume changes were identical to those observed in normal hyposmotic medium. In most cells, a rise in intracellular Ca 2ϩ concentration ([Ca 2ϩ ]i) during hyposmotic stimulation was dependent on the availability of extracellular Ca 2ϩ , although small transient increases in [Ca 2ϩ ]i were sometimes observed upon introduction of Ca 2ϩdeleted media of the same or reduced osmolality. These results indicate that an increase in cell size is a critical step in the transduction of an osmotic signal into PRL release and that the hyposmotically induced increase in PRL release is greatly dependent on extracellular Ca 2ϩ . osmoreception; signal transduction; regulatory volume decrease IN MANY EURYHALINE FISH, including the tilapia (Oreochromis mossambicus), prolactin (PRL) plays a central role in freshwater osmoregulation. By acting on osmoregulatory surfaces, PRL stimulates ion retention and decreases water influx . Consistent with its osmoregulatory activity, PRL release from the tilapia pituitary increases as extracellular osmolality is reduced both in vivo and in vitro (8, 25, 33, 34 , 42). Blood osmolality in freshwater-acclimated tilapia (ϳ310 mosmol/kgH 2 O) is somewhat lower than that in sea-

American Journal of Physiology, 2003

Evidence that signal transduction for osmoreception is mediated by stretch-activated ion channels... more Evidence that signal transduction for osmoreception is mediated by stretch-activated ion channels in tilapia. plays a central role in the freshwater osmoregulation of teleost fish, including the tilapia (Oreochromis mossambicus). Consistent with this action, PRL release from the tilapia pituitary increases as extracellular osmolality is reduced both in vitro and in vivo. Dispersed tilapia PRL cells were incubated in a perfusion chamber that allowed simultaneous measurements of cell volume and PRL release. Intracellular Ca 2ϩ concentrations were measured from fura 2-loaded PRL cells treated in a similar way. Gadolinium (Gd 3ϩ ), known to block stretch-activated cation channels, inhibited hyposmotically induced PRL release in a dose-related manner without preventing cell swelling. Nifedipine, an L-type Ca 2ϩ channel blocker, did not prevent the increase in PRL release during hyposmotic stimulation. A high, depolarizing concentration of KCl induced a transient and marked increase of intracellular Ca 2ϩ and release of PRL but did not prevent the rise in intracellular Ca 2ϩ and PRL release evoked by exposure to hyposmotic medium. These findings suggest that a decrease in extracellular osmolality stimulates PRL release through the opening of stretchactivated ion channels, which allow extracellular Ca 2ϩ to enter the cell when it swells.

General and Comparative Endcorinology, 2013

Prolactin (PRL) cells of the Mozambique tilapia, Oreochromis mossambicus, are osmoreceptors by vi... more Prolactin (PRL) cells of the Mozambique tilapia, Oreochromis mossambicus, are osmoreceptors by virtue of their intrinsic osmosensitivity coupled with their ability to directly regulate hydromineral homeostasis through the actions of PRL. Layered upon this fundamental osmotic reflex is an array of endocrine control of PRL synthesis and secretion. Consistent with its role in fresh water (FW) osmoregulation, PRL release in
tilapia increases as extracellular osmolality decreases. The hyposmotically-induced release of PRL can be enhanced or attenuated by a variety of hormones. Prolactin release has been shown to be stimulated by gonadotropin-releasing hormone (GnRH), 17-b-estradiol (E2), testosterone (T), thyrotropin-releasing hormone (TRH), atrial natriuretic peptide (ANP), brain-natriuretic peptide (BNP), C-type natriuretic peptide (CNP), ventricular natriuretic peptide (VNP), PRL-releasing peptide (PrRP), angiotensin II (ANG II), leptin, insulin-like growth factors (IGFs), ghrelin, and inhibited by somatostatin (SS), urotensin-II (U-II), dopamine, cortisol, ouabain and vasoactive intestinal peptide (VIP). This review is aimed at providing an overview of the hypothalamic and extra-hypothalamic hormones that regulate PRL release in euryhaline Mozambique tilapia, particularly in the context on how they may modulate osmoreception, and mediate the multifunctional actions of PRL. Also considered are the signal transduction pathways through which these secretagogues regulate PRL cell function.

Selenoproteins are ubiquitously expressed, act on a variety of physiological redox-related proces... more Selenoproteins are ubiquitously expressed, act on a variety of physiological redox-related processes, and are mostly regulated by selenium levels in animals. To date, the expression of most selenoproteins has not been verified in euryhaline fish models. The Mozambique tilapia, Oreochromis mossambicus, a euryhaline cichlid fish, has a high tolerance for changes in salinity and survives in fresh water (FW) and seawater (SW) environments which differ greatly in selenium availability. In the present study, we searched EST databases for cichlid selenoprotein mRNAs and screened for their differential expression in FW and SW-acclimated tilapia. The expression of mRNAs encoding iodothyronine deiodinases 1, 2 and 3 (Dio1, Dio2, Dio3), Fep15, glutathione peroxidase 2, selenoproteins J, K, L, M, P, S, and W, was measured in the brain, eye, gill, kidney, liver, pituitary, muscle, and intraperitoneal white adipose tissue. Gene expression of selenophosphate synthetase 1, Secp43, and selenocysteine lyase, factors involved in selenoprotein synthesis or in selenium metabolism, were also measured. The highest variation in selenoprotein and synthesis factor mRNA expression between FW-and SW-acclimated fish was found in gill and kidney. While the branchial expression of Dio3 was increased upon transferring tilapia from SW to FW, the inverse effect was observed when fish were transferred from FW to SW. Protein content of Dio3 was higher in fish acclimated to FW than in those acclimated to SW. Together, these results outline tissue distribution of selenoproteins in FW and SW-acclimated tilapia, and indicate that at least Dio3 expression is regulated by environmental salinity.

We assessed if leptin, a cytokine hormone known to enhance energy expenditure by promoting lipid ... more We assessed if leptin, a cytokine hormone known to enhance energy expenditure by promoting lipid and carbohydrate catabolism in response to physiologic stress, might directly regulate cellular glycolysis. A transcriptomic analysis of prolactin cells in the tilapia (Oreochromis mossambicus) pituitary rostral pars distalis (RPD) revealed that recombinant leptin (rtLep) differentially regulates 1,995 genes, in vitro. Machine learning algorithms and clustering analyses show leptin influences numerous cellular gene networks including metabolism; protein processing, transport, and metabolism; cell cycle and the hypoxia response. Leptin stimulates transcript abundance of the glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase (gapdh) in a covariate manner to the hypoxic stress gene network. Orthogonal tests confirm that rtLepA dose-dependently increases gapdh gene expression in the RPD along with transcript abundance of 6-phosphofructo-1-kinase (pfk1), the rate limiting glycolytic enzyme. Functional testing demonstrated that leptin stimulates PFK activity and glycolytic output, while Stattic (a STAT3 blocker) was sufficient to suppress these responses, indicating leptin stimulates glycolysis through a STAT3-dependent mechanism. Leptin also stimulated pfk1 gene expression and lactate production in primary hepatocyte incubations in a similar manner to those shown for the pituitary RPD. This work characterizes a critical metabolic action of leptin to directly stimulate glycolysis across tissue types in a teleost model system, and suggest that leptin may promote energy expenditure, in part, by stimulating glycolysis. These data in a teleost fish, suggest that one of leptin's ancient, highly-conserved functions among vertebrates may be stimulation of glycolysis to facilitate the energetic needs associated with various stressors.

Prolactin (PRL) cells from a teleost Wsh, the tilapia, Oreochromis mossambicus, facilitate the di... more Prolactin (PRL) cells from a teleost Wsh, the tilapia, Oreochromis mossambicus, facilitate the direct study of osmoreception. The release of two prolactins, PRL 188 and PRL 177 , which act in freshwater osmoregulation in teleost Wsh, rises in vitro within 5 min after extracellular osmolality falls. An increase in cell size accompanied this rise. Cell size and PRL release also increased, albeit more slowly, following the partial replacement of medium NaCl (55 mOsmolal) with an equivalent concentration of urea, a membranepermeant molecule. Similar replacement using mannitol, which is membrane-impermeant, elicits no response. These Wndings suggest that osmoreception is linked to changes in cell volume rather than to extracellular osmolality per se. 

Frontiers in Aging, 2021

General and Comparative Endocrinology, 2022

General and Comparative Endocrinology, 2023

Comparative Biochemistry and Physiology, 2022

American Journal of Physiology, 2022

General and Comparative Endocrinology, 2002

Cellular Physiology and Biochemistry, 2002

American Journal of Physiology, 2003

General and Comparative Endcorinology, 2013