The transfer of thyroxine from the mother to the young of the marsupials, the bandicoot (Isoodon macrourus) and the possum (Trichosurus vulpecula)

doi:10.1016/0300-9629(92)90285-X

Comparative Biochemistry and Physiology Part A: Physiology

Volume 103, Issue 3, November 1992, Pages 541-543

Comparative Biochemi...

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Abstract

1.
1. The young of the bandicoot and possum are of similar weight at birth (200–250 mg) but by day 50 post-partum have weights of 100 and 20 g, respectively. The aim of this study was to determine whether the disparate growth rate was associated with a difference in the transfer of thyroxine from mother to young.
2.
2. Radioactive thyroxine was injected intramuscularly into the lactating female and 24 hr later a blood sample was obtained from the mother and the pouch young removed. The amount of radioactive thyroxine remaining in the blood and within the young was determined.
3.
3. The data obtained indicated that milk is a source of thyroid hormones in early pouch life.
4.
4. The hypothesis that greater quantities of thyroxine are transferred in the milk of bandicoots than that of brushtail possums is not supported.

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Breeding season and litter size of the bandicoot Isoodon macrourus (Marsupialia; Peramelidae), in captivity
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Comparative studies on the hormonal profiles of progesterone and prostaglandin F metabolite in the possum Trichosurus vulpecula
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Organ development in some newborn marsupials with particular reference to the rat kangeroos
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Evolutionary implication of macro-podid organogenesis
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Thyroid hormones during development of a marsupial, the tammar wallaby, Macropus eugenii
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There are more references available in the full text version of this article.

Cited by (17)

Endocrinology of osmoregulation and thermoregulation of Australian desert tetrapods: A historical perspective
2017, General and Comparative Endocrinology
Citation Excerpt :
Increasing or decreasing thyroid hormone input can change BMR by about 50% (Somogyi et al., 2011). The majority of the work examining thyroid hormone function in Australian marsupials has involved mesic species such as the tammar wallaby, Tasmanian bettong (Bettongia gaimardi), potoroo (Potorous tridactylus), northern brown bandicoot (Isoodon macrourus) and brushtail possum (Trichosurus vulpecula; e.g. Gemmell and Sernia, 1992; Janssens et al., 1990; Nicol, 1977; Richardson et al., 2002; Rose and Kuswanti, 2004; Setchell, 1974; Sernia et al., 1997), presumably due to their ready availability near major research institutions, which are generally situated in coastal cities, and contribute little knowledge concerning adaptation to desert environments. However, Richardson et al. (2005) included the arid-habitat fat-tailed dunnart (Sminthopsis crassicaudata) in their study of the evolution of thyroxine-binding plasma proteins, and were the first to determine that an Australian polyprotodont marsupial synthesises transthyretin (one of three thyroid hormone distributor proteins that assist in the transport of thyroid hormones to the sites of action via the bloodstream) in its liver during development, in addition to thyroxine-binding globulin already identified in diprotodont pouch young.
Many Australian tetrapods inhabit desert environments characterised by low productivity, unpredictable rainfall, high temperatures and high incident solar radiation. Maintaining a homeostatic milieu intérieur by osmoregulation and thermoregulation are two physiological challenges faced by tetrapods in deserts, and the endocrine system plays an important role in regulating these processes. There is a considerable body of work examining the osmoregulatory role of antidiuretic hormones for Australian amphibians, reptiles and mammals, with particular contributions concerning their role and function for wild, free-living animals in arid environments. The osmoregulatory role of the natriuretic peptide system has received some attention, while the role of adrenal corticosteroids has been more thoroughly investigated for reptiles and marsupials. The endocrinology of thermoregulation has not received similar attention. Reptiles are best-studied, with research examining the influence of arginine vasotocin and melatonin on body temperature, the role of prostaglandins in heart rate hysteresis and the effect of melanocyte-stimulating hormone on skin reflectivity. Australian mammals have been under-utilised in studies examining the regulation, development and evolution of endothermy, and there is little information concerning the endocrinology of thermoregulation for desert species. There is a paucity of data concerning the endocrinology of osmoregulation and thermoregulation for Australian desert birds. Studies of Australian desert fauna have made substantial contributions to endocrinology, but there is considerable scope for further research. A co-ordinated approach to examine arid-habitat adaptations of the endocrine system in an environmental and evolutionary context would be of particular value.
Expression of the mammary gland-specific tammar wallaby early lactation protein gene is maintained in vitro in the absence of prolactin
2014, Molecular and Cellular Endocrinology
Citation Excerpt :
For these tammar explant studies, there was no significant difference between the IHCPRL and IHCPRLT3E2 or IHCPRLT3E2 and IHCPRLE2 treatments for either ELP, WAP or LGB expression, suggesting that neither T3 nor E2 affect in vitro tammar milk protein gene expression, with the exception of WAP expression in Phase 1 explants (Simpson et al., 2000). However, thyroid hormones delivered via milk may be critical for the survival of the tammar pouch young which does not have an active thyroid gland and is incapable of thermoregulation until ∼d180 pp (Gemmell and Sernia, 1992; Richardson et al., 2002). During tammar lactation, changes in hormone sensitivity, and autocrine and paracrine factors (Hendry et al., 1998; Nicholas et al., 1995) may affect mammary gland milk protein gene expression.
Marsupial ELP (early lactation protein) and its eutherian orthologue, CTI (colostrum trypsin inhibitor) are expressed in the mammary gland only for the first 100 days postpartum (Phase 2A) in the tammar wallaby and during the bovine and canine colostrogenesis period 24–36 h postpartum respectively. The factors which regulate temporal ELP and CTI expression are unknown. A tammar mammary gland explant culture model was used to investigate ELP gene regulation during pregnancy and early- and mid-lactation (Phase 1, 2A and 2B respectively). Tammar ELP expression could only be manipulated in explants in vitro if the gene was already expressed in vivo. ELP expression was maximal in Phase 1 explants treated with lactogenic hormones (insulin, hydrocortisone and prolactin), but unlike LGB (β-lactoglobulin), ELP expression was maintained in insulin or insulin and hydrocortisone over a 12-day culture period. In contrast, ELP was down-regulated when cultured without hormones. ELP could not be induced in explants cultured from mid-lactation which suggested that transcriptional repressors may prevent ELP expression during this period.
Marsupial models for understanding evolution of thyroid hormone distributor proteins
2008, Molecular and Cellular Endocrinology
Marsupials are a group of mammals that are under-exploited, in particular in developmental and evolutionary studies of biological systems. In this review, the roles that marsupials have played in elucidating the evolution of thyroid hormone distribution systems are summarised. Marsupials are born at very early developmental stages, and most development occurs during lactation rather than in utero. Studying thyroid hormone distribution systems during marsupial development, in addition to comparing the two Orders of marsupials, gave clues as to the selection pressures acting on the hepatic gene expression of transthyretin (TTR), one of the major thyroid hormone distributor proteins in blood. The structure of TTR in marsupials is intermediate between that of avian/reptilian TTRs and eutherian (“placental mammalian”) TTRs. Consequently, the function of marsupial TTR is intermediate between those of avian/reptilian TTRs and eutherian TTRs. Thus, in some respects marsupials can be considered as “missing links” in vertebrate evolution.
Proteomic analysis of early lactation milk of the tammar wallaby (Macropus eugenii)
2007, Comparative Biochemistry and Physiology - Part D: Genomics and Proteomics
We report the successful use of 2D electrophoresis, MALDI MS/MS and chemical derivatisation protocols of guanidination and sulfonation to identify over 100 protein spots present in early marsupial milk (tammar wallaby) at 40 days lactation, where a limited translated genomic database is publicly available for cross species matching and protein identification. Of the proteins identified, 25 matched to 6 existing marsupial milk protein sequences in the NCBI database; another 6 were identified with high confidence to other mammals and have not previously been identified in marsupial milk. By using chemical derivatisation, the reliable identification of a further 81 proteins was achieved. The identified proteins could be grouped into three main functional categories — transport, nutrition and immune protection. All these proteins play a potential role in determining growth and immunological protection of the highly altricial marsupial young at 40 days after birth.
Thyroid function and the development of endothermy in a marsupial, the Tasmanian bettong, Bettongia gaimardi (Demarest 1822)
2004, General and Comparative Endocrinology
The Tasmanian bettong (Bettongia gaimardi) is a small rat-kangaroo (marsupial) found only in Tasmania, Australia. The duration of pouch life is 15 weeks. Adults and older young display non-shivering thermogenesis and this paper examines the role of thyroxine in the development of endothermy in pouch young. Free thyroxine (T4) concentrations varied throughout pouch life. The mean (± SE) concentration was 6.2 ± 1.9 pmol L⁻¹ in week 7, increased and peaked at 19.2 ± 4.3 pmol L⁻¹ in week 12, and declined to 5.6 ± 0.4 pmol L⁻¹ by week 20. This was similar to adult levels (3.2 ± 3.8 pmol L⁻¹). These concentrations showed significant differences. From pouch week 12 onwards, T4 injection raised oxygen consumption. Maximum levels of VO₂ after T4 injection occurred at weeks 14–15. Although adult levels were lower, the increase in adult oxygen consumption after T4 injection was about 50%. Peak free T4 levels and metabolic responses to nor-adrenalin occur at week 12 and we hypothesize that thyroid hormone may facilitate the development of adrenergic-receptors in this species. The data presented in the paper further attest to the likely important role of the thyroid gland in the development of endothermy in marsupial pouch young.
Developmental profile of thyroid hormone distributor proteins in a marsupial, the tammar wallaby Macropus eugenii
2002, General and Comparative Endocrinology
The ontogeny of thyroxine distributor proteins in serum of the marsupial Macropus eugenii (tammar wallaby) was investigated from day 3 after birth until adulthood. The thyroxine distributor proteins in the serum of adult M. eugenii are transthyretin and albumin. Northern analysis of RNA prepared from liver showed that transthyretin mRNA levels were initially high (about adult levels at the earliest ages tested), reduced to about 60% adult levels (between days 50 and 150), and then steadily increased to adult levels (by days 200 to 250). Albumin mRNA levels were initially about 50% of adult levels (day 3) and steadily rose to 90% of adult levels by days 175 to 220. A globulin, “wallaby thyroxine-binding protein” (W-TBP), bound [¹²⁵I]thyroxine from day 3 until about day 200. Of the protein-bound thyroxine, the proportion bound by transthyretin had a similar pattern to the transthyretin mRNA levels. From day 26 onward, about half of the protein-bound thyroxine was bound to albumin. On day 3, less than 10% was bound to W-TBP and the proportion steadily increased to a maximum of about 46% by about day 120 and then reduced to undetectable levels by around day 250. The developmentally regulated W-TBP was present throughout pouch life, when the pouch young is dependent on obtaining thyroxine required for normal growth and development from the mother. After the young tammar wallaby leaves its mother's pouch, a time when it has reached a level of physiological development approximately equivalent to that at the time of birth in precocious eutherian mammals such as cattle and sheep, W-TBP was no longer detected as a thyroxine distributor protein in serum.

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Comparative Biochemistry and Physiology Part A: Physiology

Abstract

References (20)

The development of thermoregulation and thyroid function in the marsupial Macropus eugenii (Desmarest)

Comp. Biochem. Physiol.

Breeding bandicoots in Brisbane (Marsupialia: Peramelidae)

Aust. Mammal.

Breeding season and litter size of the bandicoot Isoodon macrourus (Marsupialia; Peramelidae), in captivity

Aust. Mammal.

Comparative studies on the hormonal profiles of progesterone and prostaglandin F metabolite in the possum Trichosurus vulpecula

The development of thermoregulation and the emergence from the pouch of the marsupial bandicoot, Isoodon macrourus

Physiol. Zool.

The uniformity of growth within the litter of the marsupial Isoodon macrourus

Growth

Osteogenesis in two marsupial species, the bandicoot Isoodon macrourus, and the possum Trichosurus vulpecula

J. Anat.

Organ development in some newborn marsupials with particular reference to the rat kangeroos

Evolutionary implication of macro-podid organogenesis

Thyroid hormones during development of a marsupial, the tammar wallaby, Macropus eugenii

J. Endocr.

Cited by (17)

Endocrinology of osmoregulation and thermoregulation of Australian desert tetrapods: A historical perspective

Expression of the mammary gland-specific tammar wallaby early lactation protein gene is maintained in vitro in the absence of prolactin

Marsupial models for understanding evolution of thyroid hormone distributor proteins

Proteomic analysis of early lactation milk of the tammar wallaby (Macropus eugenii)

Thyroid function and the development of endothermy in a marsupial, the Tasmanian bettong, Bettongia gaimardi (Demarest 1822)

Developmental profile of thyroid hormone distributor proteins in a marsupial, the tammar wallaby Macropus eugenii