Early down-regulation of milk production after weaning by pup removal and prior to involution in mouse mammary glands

Cell and Tissue Research

Volumn 359, Issue 2, 2015, Pages 643-653

  Uejyo, Takaaki ^a   Kuki, Chinatsu ^a   Oyama, Shoko ^a   Kumura, Haruto ^a   Kobayashi, Ken ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Alveolar epithelial cell; Involution; Lactation; Mammary gland; Weaning

Indexed keywords

AQUAPORIN 3; CASPASE 3; FAT DROPLET; STAT3 PROTEIN; STAT5 PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRIACYLGLYCEROL; CASEIN; MEMBRANE PROTEIN; PERILIPIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; AQP3 GENE; ARTICLE; BREAST EPITHELIUM CELL; CELL COUNT; CELL DEATH; CELL FUNCTION; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; GENE EXPRESSION REGULATION; INVOLUTION; LACTATION; LIPOGENESIS; MAMMARY GLAND; MILK PRODUCTION; MOUSE; NEWBORN; NONHUMAN; NUTRIENT UPTAKE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; SREBP1 GENE; SUCKING; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; WEANING; ANIMAL; BIOLOGICAL MODEL; FEMALE; GROWTH, DEVELOPMENT AND AGING; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MILK; TIME; UDDER;

ANIMALS; ANIMALS, NEWBORN; CASEINS; CASPASE 3; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION; MAMMARY GLANDS, ANIMAL; MEMBRANE PROTEINS; MICE, INBRED ICR; MILK; MODELS, BIOLOGICAL; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR; TIME FACTORS; WEANING;

EID: 84925533828     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-014-2013-7     Document Type: Article

References (43)

1. Anderson SM, Rudolph MC, McManaman JL, Neville MC (2007) Key stages in mammary gland development. Secretory activation in the mammary gland: it’s not just about milk protein synthesis! Breast Cancer Res 9:204
2. Ayadi M, Hammadi M, Khorchani T, Barmat A, Atigui M, Caja G (2009) Effects of milking interval and cisternal udder evaluation in Tunisian Maghrebi dairy dromedaries (Camelus dromedarius L.). J Dairy Sci 92:1452–1459
3. Ben Chedly H, Lacasse P, Marnet PG, Boutinaud M (2013) The decrease in milk yield during once daily milking is due to regulation of synthetic activity rather than apoptosis of mammary epithelial cells in goats. Animal 7:124–133
4. Blanchard AA, Watson PH, Shiu RP, Leygue E, Nistor A, Wong P, Myal Y (2006) Differential expression of claudin 1, 3, and 4 during normal mammary gland development in the mouse. DNA Cell Biol 25:79–86
5. Brew K, Vanaman TC, Hill RL (1968) The role of alpha-lactalbumin and the A protein in lactose synthetase: a unique mechanism for the control of a biological reaction. Proc Natl Acad Sci U S A 59:491–497
6. Brisken C (2002) Hormonal control of alveolar development and its implications for breast carcinogenesis. J Mammary Gland Biol Neoplasia 7:39–48
7. Brisken C, Socolovsky M, Lodish HF, Weinberg R (2002) The signaling domain of the erythropoietin receptor rescues prolactin receptor-mutant mammary epithelium. Proc Natl Acad Sci U S A 99:14241–14245
8. Camps M, Vilaro S, Testar X, Palacin M, Zorzano A (1994) High and polarized expression of GLUT1 glucose transporters in epithelial cells from mammary gland: acute down-regulation of GLUT1 carriers by weaning. Endocrinology 134:924–934
9. Chat S, Layani S, Mahaut C, Henry C, Chanat E, Truchet S (2011) Characterisation of the potential SNARE proteins relevant to milk product release by mouse mammary epithelial cells. Eur J Cell Biol 90:401–413
10. Clarkson RW, Heeley JL, Chapman R, Aillet F, Hay RT, Wyllie A, Watson CJ (2000) NF-kappaB inhibits apoptosis in murine mammary epithelia. J Biol Chem 275:12737–12742
11. Clarkson RW, Boland MP, Kritikou EA, Lee JM, Freeman TC, Tiffen PG, Watson CJ (2006) The genes induced by signal transducer and activators of transcription (STAT)3 and STAT5 in mammary epithelial cells define the roles of these STATs in mammary development. Mol Endocrinol 20:675–685
12. Connelly L, Barham W, Pigg R, Saint-Jean L, Sherrill T, Cheng DS, Chodosh LA, Blackwell TS, Yull FE (2010) Activation of nuclear factor kappa B in mammary epithelium promotes milk loss during mammary development and infection. J Cell Physiol 222:73–81
13. Han LQ, Li HJ, Wang YY, Zhu HS, Wang LF, Guo YJ, Lu WF, Wang YL, Yang GY (2010) mRNA abundance and expression of SLC27A, ACC, SCD, FADS, LPIN, INSIG, and PPARGC1 gene isoforms in mouse mammary glands during the lactation cycle. Genet Mol Res 9:1250–1257
14. Hughes K, Wickenden JA, Allen JE, Watson CJ (2012) Conditional deletion of Stat3 in mammary epithelium impairs the acute phase response and modulates immune cell numbers during post-lactational regression. J Pathol 227:106–117
15. Iavnilovitch E, Groner B, Barash I (2002) Overexpression and forced activation of stat5 in mammary gland of transgenic mice promotes cellular proliferation, enhances differentiation, and delays postlactational apoptosis. Mol Cancer Res 1:32–47
16. Kobayashi K, Oyama S, Numata A, Rahman MM, Kumura H (2013a) Lipopolysaccharide disrupts the milk-blood barrier by modulating claudins in mammary alveolar tight junctions. PLoS ONE 8:e62187
17. Kobayashi K, Oyama S, Uejyo T, Kuki C, Rahman MM, Kumura H (2013b) Underlying mechanisms involved in the decrease of milk secretion during Escherichia coli endotoxin induced mastitis in lactating mice. Vet Res 44:119
18. Kobayashi K, Uejyo T, Oyama S, Rahman MM, Kumura H (2013c) Histological analysis of mammary gland remodeling caused by lipopolysaccharide in lactating mice. Cell Tissue Res 354:495–506
19. Kreuzaler PA, Staniszewska AD, Li W, Omidvar N, Kedjouar B, Turkson J, Poli V, Flavell RA, Clarkson RW, Watson CJ (2011) Stat3 controls lysosomal-mediated cell death in vivo. Nat Cell Biol 13:303–309
20. Laspiur JP, Burton JL, Weber PS, Kirkwood RN, Trottier NL (2004) Short communication: amino acid transporters in porcine mammary gland during lactation. J Dairy Sci 87:3235–3237
21. Li M, Liu X, Robinson G, Bar-Peled U, Wagner KU, Young WS, Hennighausen L, Furth PA (1997) Mammary-derived signals activate programmed cell death during the first stage of mammary gland involution. Proc Natl Acad Sci U S A 94:3425–3430
22. Liu X, Robinson GW, Wagner KU, Garrett L, Wynshaw-Boris A, Hennighausen L (1997) Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev 11:179–186
23. Lund LR, Romer J, Thomasset N, Solberg H, Pyke C, Bissell MJ, Dano K, Werb Z (1996) Two distinct phases of apoptosis in mammary gland involution: proteinase-independent and -dependent pathways. Development 122:181–193
24. Markov AG, Ruhle HJ (1992) The influence of exogenous oxytoxin on labelling of secretory epithelium of mouse mammary gland by [3H]leucine, evidenced by autoradiography. Exp Clin Endocrinol 100:112–116
25. Matsuzaki T, Machida N, Tajika Y, Ablimit A, Suzuki T, Aoki T, Hagiwara H, Takata K (2005) Expression and immunolocalization of water-channel aquaporins in the rat and mouse mammary gland. Histochem Cell Biol 123:501–512
26. Monks J, Smith-Steinhart C, Kruk ER, Fadok VA, Henson PM (2008) Epithelial cells remove apoptotic epithelial cells during post-lactation involution of the mouse mammary gland. Biol Reprod 78:586–594
27. Nakatani H, Aoki N, Nakagawa Y, Jin-No S, Aoyama K, Oshima K, Ohira S, Sato C, Nadano D, Matsuda T (2006) Weaning-induced expression of a milk-fat globule protein, MFG-E8, in mouse mammary glands, as demonstrated by the analyses of its mRNA, protein and phosphatidylserine-binding activity. Biochem J 395:21–30
28. Nakatani H, Yasueda T, Oshima K, Okajima T, Nadano D, Flint DJ, Matsuda T (2013) Post-weaning increases in the milk-fat globule EGF-factor VIII on fat globules in mouse milk and in the uptake of the fat globules by HC11 mammary epithelial cells. J Biochem 153:31–41
29. Neville MC, Morton J, Umemura S (2001) Lactogenesis. The transition from pregnancy to lactation. Pediatr Clin N Am 48:35–52
30. Nudda A, Bencini R, Mijatovic S, Pulina G (2002) The yield and composition of milk in Sarda, Awassi, and Merino sheep milked unilaterally at different frequencies. J Dairy Sci 85:2879–2884
31. Pitelka DR, Hamamoto ST, Duafala JG, Nemanic MK (1973) Cell contacts in the mouse mammary gland. I. Normal gland in postnatal development and the secretory cycle. J Cell Biol 56:797–818
32. Quaglino A, Salierno M, Pellegrotti J, Rubinstein N, Kordon EC (2009) Mechanical strain induces involution-associated events in mammary epithelial cells. BMC Cell Biol 10:55
33. Rudolph MC, McManaman JL, Hunter L, Phang T, Neville MC (2003) Functional development of the mammary gland: use of expression profiling and trajectory clustering to reveal changes in gene expression during pregnancy, lactation, and involution. J Mammary Gland Biol Neoplasia 8:287–307
34. Rudolph MC, Neville MC, Anderson SM (2007) Lipid synthesis in lactation: diet and the fatty acid switch. J Mammary Gland Biol Neoplasia 12:269–281
35. Rudolph MC, Monks J, Burns V, Phistry M, Marians R, Foote MR, Bauman DE, Anderson SM, Neville MC (2010) Sterol regulatory element binding protein and dietary lipid regulation of fatty acid synthesis in the mammary epithelium. Am J Physiol Endocrinol Metab 299:E918–E927
36. Schwertfeger KL, McManaman JL, Palmer CA, Neville MC, Anderson SM (2003) Expression of constitutively activated Akt in the mammary gland leads to excess lipid synthesis during pregnancy and lactation. J Lipid Res 44:1100–1112
37. Scribner KC, Wellberg EA, Metz RP, Porter WW (2011) Singleminded-2s (Sim2s) promotes delayed involution of the mouse mammary gland through suppression of Stat3 and NFkappaB. Mol Endocrinol 25:635–644
38. Stelwagen K, Farr VC, McFadden HA, Prosser CG, Davis SR (1997) Time course of milk accumulation-induced opening of mammary tight junctions, and blood clearance of milk components. Am J Physiol 273:R379–R386
39. Strange R, Li F, Saurer S, Burkhardt A, Friis RR (1992) Apoptotic cell death and tissue remodelling during mouse mammary gland involution. Development 115:49–58
40. Teglund S, McKay C, Schuetz E, van Deursen JM, Stravopodis D, Wang D, Brown M, Bodner S, Grosveld G, Ihle JN (1998) Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 93:841–850
41. Tolkunov YA, Markov AG (1997) Integrity of the secretory epithelium of the lactating mouse mammary gland during extended periods after suckling. J Dairy Res 64:39–45
42. Watson CJ (2006) Involution: apoptosis and tissue remodelling that convert the mammary gland from milk factory to a quiescent organ. Breast Cancer Res 8:203
43. Watson CJ, Kreuzaler PA (2011) Remodeling mechanisms of the mammary gland during involution. Int J Dev Biol 55:757–762