Recent progress of porcine milk components and mammary gland function

Abstract

As the only nutritional source for newborn piglets, porcine colostrum and milk contain critical nutritional and immunological components including carbohydrates, lipids, and proteins (immunoglobulins). However, porcine milk composition is more complex than these three components. Recently, scientists identified additional and novel components of sow colostrum and milk, including exosomes, oligosaccharides, and bacteria, which possibly act as biological signals and modulate the intestinal environment and immune status in piglets and later in life. Evaluation of these nutritional and non-nutritional components in porcine milk will help better understand the nutritional and biological function of porcine colostrum and milk. Furthermore, some important functions of the porcine mammary gland have been reported in recent published literature. These preliminary studies hypothesized how glucose, amino acids, and fatty acids are transported from maternal blood to the porcine mammary gland for milk synthesis. Therefore, we summarized recent reports on sow milk composition and porcine mammary gland function in this review, with particular emphasis on macronutrient transfer and synthesis mechanisms, which might offer a possible approach for regulation of milk synthesis in the future.

Keywords: Bioactive components; Fat; Lactose; Mammary gland; Porcine milk; Protein.

Fig. 1

Composition of sow milk throughout lactation. Note: a. Porcine milk composition in 1980s. These data were summarized by Klobasa et al. [103]. b. Porcine milk composition in 2010s. References used to calculate averages of milk composition in last 10 years: Kim et al. [104], Tian et al. [105], Bai et al. [106], Wang et al. [107], Shen et al. [108], Decaluwe et al. [109], Wang et al. [110], Samanc et al. [111], Loisel et al. [112], Krogh et al. [113], Flummer and Theil [114], Zhao et al. [115], Velayudhan and Nyachoti [116], Rosero et al. [117], Farmer et al. [118], Park et al. [119], Wang et al. [120]

Fig. 2

Lactose synthesis pathway in porcine mammary gland. Note: Glucose is taken up by the porcine mammary gland through membrane glucose transporters (possibly GLUT1). In the cytoplasm, after glucose is converted into glucose-6-phosphate, it will be further converted into UDP-galactose by a series of enzymes: PGM, UGP2, GALT, and GALE. Subsequently, glucose and UDP-galactose in the cytoplasm is transported into the Golgi bodies by GLUT1 (possibly) and SLC35A2, respectively. Finally, glucose and UDP-galactose are synthesized into lactose by LALBA and B4GALT1 in the Golgi bodies. After the initation of lactation, mRNA of enzymes is increased 2-fold or more are shown in light purple; those increasing 1.5-to1.9-fold are colored light red, and those expression increase or decrease less than 1.5-fold are shown in light gray. Abbreviation: GLUT1, glucose transporter-1; PGM, phosphoglycerate mutase; UGP2: UDP-glucose pyrophosphorylase 2; GALT, galactose-1-phosphate uridyltransferase; GALE, e UDP-glucose 4-epimerase gene; LALBA, alpha-lactalbumin gene; β-1,4-galactosyltransferase

Fig. 3

Milk protein synthesis pathway in porcine mammary gland. Note: Amino acids from blood are taken up by the porcine mammary gland through cationic amino acid transporters (CAT-1 and CAT-2B), neutral amino acid transporters (ASCT1, LAT2 and SNAT2), cationic and neutral amino acid transporters (b^0,+AT, ATB^0,+,y⁺LAT1, y⁺LAT2), and anionic amino acid transporters (EAAC1 and EAAC3). Amino acid uptake by the porcine mammary gland can be divided into three levels: high level (leucine, arginine and lysine), middle level (valine, isoleucine, threonine, phenylalanine), and low level (tyrosine, methionine and histidine). Subsequently, amino acids are converted into caseins and whey proteins, such as, α_S1-casein (CSN1S1), α_S2-casein (CSN1S2), β-casein (CSN2), κ-casein (CSN3), α-lactalbumin (LALBA), whey acidic protein (WAP), LTF (lactotransferrin), ALB (albumin). Abbreviations: CAT1, cationic amino acid transporter1; CAT-2B, cationic amino acid transporter 2B; ASCT1, system ASC neutral amino acid transporter 1; LAT2, L-type amino acid transporter 2; SNAT2, sodium-coupled neutral amino acid transporter 2; b^0,+AT, b^0,+ amino acid transporter; ATB^0,+, B^0,+amino acid transporter; y⁺LAT1, y⁺-type amino acid transporter 1; y⁺LAT2, y⁺-type amino acid transporter 2; EAAC1, excitatory amino-acid carrier 1; EAAC3, excitatory amino-acid carrier 3

Fig. 4

Components of whey protein in colostrum and milk. Note: Data are summarized from the information provided by Hurley [93]

Fig. 5

Lipid synthesis pathway in porcine mammary gland. Note: LCFA the enter porcine mammary gland, facilitated by transport proteins (mainly CD36), and are converted into their activated form LC-acyl-CoA, with the help of ACSL. Cytosolic LC-acyl-CoA is transported to the endoplasmic reticulum membrane by FABP3 and esterified there to glycerol-3-phosphate to produce LPA by GPAM. In the endoplasmic reticulum, PA can be hydrolyzed with LPIN to form DAG, which then is acylated to form TAG by DGAT. Newly-formed TAG forms cytoplasmic lipid droplets in the ER membrane via incorporation. The cytoplasmic lipid droplets are then transported to the apical membrane, and eventually released into porcine milk. A series of enzymes are required to facilitate this process, of which FASN and ACACA are considered the crucial enzymes of cellular fatty acid de novo synthesis. ACACA carboxylates acetyl-CoA to form malonyl-CoA, which is further converted by FASN to fatty acids (C ≤ 16). The synthesized fatty acids then participate in TAG formation. After the initation of lactation, mRNA of enzymes is increased 5-fold or more are shown in light purple; those increasing 2-fold or more are colored light red, and those expression increase or decrease less than 2-fold are shown in light gray. Abbreviations: ACACA, acetyl-CoA carboxylase alpha; ACSL3, acyl-CoA synthetase long-chain family member 3; ACSS2, acyl-CoA synthetase short-chain family member 2; AGPAT6, 1-acyl-sn-glycerol-3-phosphate acyltransferase 6; CD36, fatty acid translocase/CD36; CLD, cytoplasmic lipid droplet; DAG, diacylglycerol; DGAT1, diacylglycerol acyltransferase 1; FABP3, fatty acid binding protein 3; FASN, fatty acid synthase; GPAM, glycerol-3-phosphate acyltransferase, mitochondrial; LCFA, long chain fatty acid; LPA, lysophosphatidic acid; LPIN2, lipin 2; MFG, milk fat globule; PA, phosphatidic acid; PLIN2, perilipin 2; PPARγ, peroxisome proliferator-activated receptor γ; SCFA, short chain fatty acid; SCD, stearoyl-CoA desaturase; TAG, triacylglycerol