Monotremes and marsupials: Comparative models to better understand the function of milk

Kuruppath, Sanjana; Bisana, Swathi; Sharp, Julie A.; Lefèvre, Christophe; Kumar, Satish; Nicholas, Kevin R.

doi:10.1007/s12038-012-9247-x

Cited by 10 publications

(4 citation statements)

References 54 publications

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“…It is quite possible to speculate the mother-to-hatchling transfer of pathogens. Milk, as the first and only source of nutrition, may play a key role in transfer of antimicrobial proteins in protecting the immunologically vulnerable young during early monotreme development (Renfree and Shaw 2001; Wong et al 2009; Kuruppath et al 2012; Bisana et al 2013). Recently, the echidna milk protein gene, EchAMP which is highly expressed in both short-beaked echidna and platypus mammary cells during lactation has been identified as an antibacterial protein which is implicated in milk protein-mediated innate immunity (Bisana et al 2013).…”

Section: Discussionmentioning

confidence: 99%

“…The newly hatched monotreme very much resembles that of new born marsupials (Renfree and Shaw 2001). In monotreme milk secretion β-lactoglobulin (Lefèvre et al 2009), transferrin (Teahan and McKenzie 1990), lysozyme (Teahan, McKenzie, Shaw, et al 1991), and WAP four-disulfide core domain 2 (Sharp et al 2007) have been identified, but not the cathelicidin protein (Whittington et al 2009; Wang et al 2011), suggesting that similar immune antimicrobial component secretion in monotreme milk could act to protect the immunocompromised hatchlings (Wong et al 2009; Kuruppath et al 2012). …”

Section: Discussionmentioning

confidence: 99%

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Monotreme Lactation Protein Is Highly Expressed in Monotreme Milk and Provides Antimicrobial Protection

Enjapoori¹,

Grant²,

Nicol³

et al. 2014

Genome Biology and Evolution

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Monotremes (platypus and echidna) are the descendants of the oldest ancestor of all extant mammals distinguished from other mammals by mode of reproduction. Monotremes lay eggs following a short gestation period and after an even briefer incubation period, altricial hatchlings are nourished over a long lactation period with milk secreted by nipple-less mammary patches located on the female’s abdomen. Milk is the sole source of nutrition and immune protection for the developing young until weaning. Using transcriptome and mass spectrometry analysis of milk cells and milk proteins, respectively, a novel Monotreme Lactation Protein (MLP) was identified as a major secreted protein in milk. We show that platypus and short-beaked echidna MLP genes show significant homology and are unique to monotremes. The MLP transcript was shown to be expressed in a variety of tissues; however, highest expression was observed in milk cells and was expressed constitutively from early to late lactation. Analysis of recombinant MLP showed that it is an N-linked glycosylated protein and biophysical studies predicted that MLP is an amphipathic, α-helical protein, a typical feature of antimicrobial proteins. Functional analysis revealed MLP antibacterial activity against both opportunistic pathogenic Staphylococcus aureus and commensal Enterococcus faecalis bacteria but showed no effect on Escherichia coli, Pseudomonas aeruginosa, Staphylococcus epidermidis, and Salmonella enterica. Our data suggest that MLP is an evolutionarily ancient component of milk-mediated innate immunity absent in other mammals. We propose that MLP evolved specifically in the monotreme lineage supporting the evolution of lactation in these species to provide bacterial protection, at a time when mammals lacked nipples.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Monotreme Lactation Protein Is Highly Expressed in Monotreme Milk and Provides Antimicrobial Protection

Enjapoori¹,

Grant²,

Nicol³

et al. 2014

Genome Biology and Evolution

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“…The composition of milk varies greatly among species, largely reflecting the nutritional needs of the neonate but also reflecting other physiological requirements, especially among the extremely altricial young of marsupials and monotremes [188][189][190]. However, the needs of the young must be balanced against those of the mother and it has been be argued that the protection of the mammary gland against ectopic or pathological calcification has been an important constraint on the composition of milk [191] because the gland goes through repeated cycles of development, lactation, and involution during the reproductive life of the female.…”

Section: Stability Of Milkmentioning

confidence: 99%

Structural Biology of Calcium Phosphate Nanoclusters Sequestered by Phosphoproteins

et al. 2020

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Biofluids that contain stable calcium phosphate nanoclusters sequestered by phosphopeptides make it possible for soft and hard tissues to co-exist in the same organism with relative ease. The stability diagram of a solution of nanocluster complexes shows how the minimum concentration of phosphopeptide needed for stability increases with pH. In the stable region, amorphous calcium phosphate cannot precipitate. Nevertheless, if the solution is brought into contact with hydroxyapatite, the crystalline phase will grow at the expense of the nanocluster complexes. The physico-chemical principles governing the formation, composition, size, structure, and stability of the complexes are described. Examples are given of complexes formed by casein, osteopontin, and recombinant phosphopeptides. Application of these principles and properties to blood serum, milk, urine, and resting saliva is described to show that under physiological conditions they are in the stable region of their stability diagram and so cannot cause soft tissue calcification. Stimulated saliva, however, is in the metastable region, consistent with its role in tooth remineralization. Destabilization of biofluids, with consequential ill-effects, can occur when there is a failure of homeostasis, such as an increase in pH without a balancing increase in the concentration of sequestering phosphopeptides.

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“…These skin secretions could provide sustenance and protection from infection for offspring and this process is still found in the egg-laying monotremes, animals whose young are produced in an immature form and require both feeding and protection. As the offspring matures, the composition of the secretion changes ( Tyndale-Biscoe and Janssens, 1988 ; Lefèvre et al, 2010 ; Kuruppath et al, 2012 ; Sharp et al, 2020 ). The development of secretory cells associated with a specific organ, the teat, appears to have occurred around 165 Mya subsequently followed by the development of the true placenta and the emergence around 148 Mya of the eutheria or placentalia ( Oftedal, 2002 , 2013 ; Lefèvre et al, 2010 ).…”

Section: Introductionmentioning

confidence: 99%

β-Lactoglobulin and Glycodelin: Two Sides of the Same Coin?

Sawyer

2021

Front. Physiol.

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The two lipocalins, β-lactoglobulin (βLg) and glycodelin (Gd), are possibly the most closely related members of the large and widely distributed lipocalin family, yet their functions appear to be substantially different. Indeed, the function of β-lactoglobulin, a major component of ruminant milk, is still unclear although neonatal nutrition is clearly important. On the other hand, glycodelin has several specific functions in reproduction conferred through distinct, tissue specific glycosylation of the polypeptide backbone. It is also associated with some cancer outcomes. The glycodelin gene, PAEP, reflecting one of its names, progestagen-associated endometrial protein, is expressed in many though not all primates, but the name has now also been adopted for the β-lactoglobulin gene (HGNC, www.genenames.org). After a general overview of the two proteins in the context of the lipocalin family, this review considers the properties of each in the light of their physiological functional significance, supplementing earlier reviews to include studies from the past decade. While the biological function of glycodelin is reasonably well defined, that of β-lactoglobulin remains elusive.

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Monotremes and marsupials: Comparative models to better understand the function of milk

Cited by 10 publications

References 54 publications

Monotreme Lactation Protein Is Highly Expressed in Monotreme Milk and Provides Antimicrobial Protection

Monotreme Lactation Protein Is Highly Expressed in Monotreme Milk and Provides Antimicrobial Protection

Structural Biology of Calcium Phosphate Nanoclusters Sequestered by Phosphoproteins

β-Lactoglobulin and Glycodelin: Two Sides of the Same Coin?

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