Characterization of Primary Cilia Distribution and Morphology During Lactation, Stasis, and Involution in the Bovine Mammary Gland

Millier, Melanie J; Singh, Kuljeet; Poole, Charles

doi:10.1002/ar.22819

Cited by 7 publications

(9 citation statements)

References 75 publications

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“…Furthermore, studies in vivo demonstrated that acute physical distension of rat mammary glands with sucrose solution accelerated the induction of apoptosis, upregulation of the apoptotic factor activated signal transducer and activator of transcription-3, and loss of the extracellular matrix factor β1-integrin and tight junction factor occludin (Phyn et al, 2007). Recently, the distribution and morphological changes in the mechanosensors primary cilia during lactation and involution implicate a role in initiating involution of the mammary gland (Millier et al, 2013).…”

Section: Discussionmentioning

confidence: 98%

The effect of milking reinitiation following extended nonmilking periods on lactation in primiparous dairy cows

Singh

Swanson

et al. 2015

Journal of Dairy Science

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In dairy cows, extended periods of nonmilking results in reduced milk secretion, modifications in milk composition, and eventually involution of the mammary glands. The aim of this study was to determine the effect of extended nonmilking periods on the recovery of milk yield and composition, and levels of prolactin and insulin-like growth factor-I in pasture-fed cows after resuming milking. Pasture-fed, primiparous, nonpregnant, Friesian dairy cows at mid lactation (mean ± standard deviation, 97 ± 2d in milk, 14.0 ± 2.5 L/d) were divided into 3 groups (n=6 per group). The cows were subjected to nonmilking periods of 7, 14, or 28d. Twice-daily milking was resumed for 7d following the nonmilking periods. Milk yield recoveries at the end of the 7-d remilking period were 91, 51, and 29% for the 7, 14, and 28-d nonmilked groups, respectively. The somatic cell count declined to less than 400,000 cells/mL by d 3 and 6 of remilking for the 7- and 14-d-nonmilked groups, respectively, but remained greater than 800,000 cells/mL in the 28-d-nonmilked group through the 7-d remilking period. By d 7 of remilking, the somatic cell count for the 7-d-nonmilked group was not different from pretrial values. Upon remilking, the milk fat content returned to pretrial values for the 7- and 14-d-nonmilked groups, although it remained lower than pretrial for the 28-d-nonmilked group. All 3 nonmilked groups had a higher milk protein content following 7d of remilking, compared with pretrial values. The lactose content returned to pretrial values for the 7-d-nonmilked group but remained lower for the 14- and 28-d-nonmilked groups. Circulating prolactin concentrations increased once remilking was resumed, compared with the pretrial and nonmilking periods. Prolactin concentrations did not majorly differ between the groups, with the levels upon 7d of remilking remaining higher than the pretrial concentrations and the nonmilked periods. Plasma concentrations of insulin-like growth factor-I increased during the nonmilking period and were greater in all 3 nonmilked groups on d 1 of remilking than pretrial values and returned to pretrial concentrations following remilking for the 7-d-nonmilked group, whereas the 14- and 28-d-nonmilked groups remained higher than the pretrial values. These data indicate that the process of involution is fully reversed after remilking following 7d of milk stasis but more extended periods of nonmilking prevent the complete recovery of lactation. However, even after 28d of milk stasis, the milk synthesis capacity of the mammary gland could still be partially recovered.

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Section: Discussionmentioning

confidence: 98%

The effect of milking reinitiation following extended nonmilking periods on lactation in primiparous dairy cows

Singh

Swanson

et al. 2015

Journal of Dairy Science

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“…In support of mechanotransduction, mammary cell stretch in vitro induces apoptotic pathways (Quaglino et al, ) and in vivo accelerates the induction of apoptosis and loss of the ECM factor β1‐integrin and the TJ protein occludin (Phyn et al, ). Furthermore, primary cilia, key signalling organelles for sensing biochemical and biophysical extracellular stimuli, have been implicated in initiating involution of the mammary gland (Millier et al, ; Biet et al, ).…”

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confidence: 99%

Tight Junction Protein Abundance and Apoptosis During Involution of Rat Mammary Glands

Phyn

Stelwagen

Davis

et al. 2017

Journal Cellular Physiology

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To examine tight junction protein abundance and apoptosis of epithelial cells at the onset of involution in rodent mammary glands, milk accumulation and mammary engorgement were induced by teat-sealing with an adhesive for 0, 6, 12, 18, 24, and 36 h (n = 6 per group) at peak lactation. In non-sealed control glands, histological analysis confirmed a lactating phenotype, indicating suckling by pups throughout the experiment. In contrast, alveoli of teat-sealed glands were distended within 6 h, with maximal luminal size observed by 12 h of non-suckling. By 18 h following teat-sealing, an involuting phenotype was observed, indicated by alveolar lumina engorged with milk vesicles and increased leukocytes. Relative to non-sealed glands, mammary apoptosis was increased in engorged glands 18 h following teat-sealing. The abundance of ZO-1 and occludin proteins was decreased in engorged glands by 12 and 18 h, respectively, following teat-sealing. In contrast, the claudin-1 22 kDa band was increased by 6 h and peaked at 12-18 h, whereas the 28 kDa band declined by 36 h, relative to controls. There were no temporal changes in ZO-1, occludin, and claudin-1 22 kDa proteins within control glands, although there were minor differences in claudin-1 28 kDa. These data indicate that intramammary milk accumulation due to cessation of milk removal is associated with mammary apoptosis. The apoptotic event is preceded by a rapid loss of abundance of ZO-1, occludin and an initial increase in claudin-1. The loss of cell-cell communication may initiate involution and apoptosis of mammary epithelial cells and is a localized intramammary event, occurring only in non-suckled glands. J. Cell. Physiol. 232: 2075-2082, 2017. © 2016 Wiley Periodicals, Inc.

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“…In the total fraction, the percentage of ciliated cells was the same in the lactation and 7-d NM groups, but was increased (P < 0.1) in the 28-d NM group compared with the lactation group (Figure 4). Nevertheless, the average depth of Z-stacks was 1.5 μm, whereas the tissue sections were 7 μm, both considerably less than the average width of a luminal SEC (Millier et al, 2013). Therefore, the proportion of cilia detected will most likely underestimate the actual biological incidence.…”

Section: Quantitative Analysis Of Pc Incidence and Orientationmentioning

confidence: 96%

“…In the bovine mammary gland, the presence of PC on SEC and MEC was first demonstrated by Nickerson (1989). More recently, PC incidence and celltype distribution and morphology have been described during lactation, milk stasis, and early involution, suggesting a potential mechanosensory role the bovine mammary gland (Millier et al, 2013).…”

Section: Introductionmentioning

confidence: 96%

Primary cilia distribution and orientation during involution of the bovine mammary gland

Biet

Poole

Stelwagen³

et al. 2016

Journal of Dairy Science

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The regulation of mammary gland involution occurs through multiple levels including environmental factors, hormones, and local intramammary signals. Primary cilia (PC) are signaling organelles that sense biochemical and biophysical extracellular stimuli and are vital for cellular and tissue function. The aim of this study was to examine the distribution, incidence, and orientation of PC. Furthermore, we determined changes in expression levels of the signal transducer and activator of transcription (STAT)6 at the onset of bovine mammary gland involution. Mammary tissue was collected from pasture-fed, primiparous, nonpregnant Friesian dairy cows at mid lactation (n=5 per group) killed 6-h after milking (lactating controls) and during involution after 7 and 28 d of nonmilking (NM). Fluorescent immunohistochemistry and confocal microscopy of tissue sections showed that PC were present on luminal secretory epithelial cells (SEC), myoepithelial cells (MEC), and stromal fibroblast cells (SFC). Furthermore, in all 3 experimental groups, different PC positions or orientations relative to the cell surface were identified on SEC and MEC, which projected toward the lumen and were either straight, bent, or deflected against the apical cell surface, whereas PC in SFC were confined to the interalveolar space. However, by 28-d NM, fewer PC projected into the luminal space and most appeared deflected or projected toward the interalveolar space. Furthermore, by 28-d NM, with the increase in stromal connective tissue, more PC were detected within the interalveolar and interlobular stroma. At 28-d NM, we observed a decrease in luminal cilia relative to the total number of cilia. The number of ciliated cells in the total fraction (SEC, MEC, and SFC) was the same for all 3 groups, although in the luminal fraction (SEC and MEC), PC per nuclei increased by 28-d NM relative to lactation. At all 3 stages, we detected variations in shape and orientation of PC within the same alveolus, with some PC projecting directly into lumen, whereas others appeared to be bent or deflected flat against the cell surface. Within each treatment, the average number of bent cilia was low, whereas the average number of deflected cilia was higher than the average number of cilia projecting directly into the lumen. Quantitative real-time reverse transcription PCR analysis showed that expression levels of milk protein genes (αS1-casein, α-lactalbumin, and κ-casein) declined and that of lactoferrin increased in the involuted mammary tissue following NM, compared with lactating controls. Although STAT6 mRNA levels did not change following NM, STAT6 protein levels did increase following 28-d NM compared with the control lactation group. In conclusion, PC were detected in all cell types in the mammary gland, and changes in orientation during involution suggest the potential for PC to play a role in signal transduction through both mechanosensation and chemosensation. Furthermore, the STAT6-mediated signaling pathway may have a role during involution of the mammary g...

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Characterization of Primary Cilia Distribution and Morphology During Lactation, Stasis, and Involution in the Bovine Mammary Gland

Cited by 7 publications

References 75 publications

The effect of milking reinitiation following extended nonmilking periods on lactation in primiparous dairy cows

The effect of milking reinitiation following extended nonmilking periods on lactation in primiparous dairy cows

Tight Junction Protein Abundance and Apoptosis During Involution of Rat Mammary Glands

Primary cilia distribution and orientation during involution of the bovine mammary gland

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