Misexpression of wingless-related MMTV integration site 5A in mouse mammary gland inhibits the milk ejection response and regulates connexin43 phosphorylation

Biology of Reproduction

Volumn 85, Issue 5, 2011, Pages 907-915

  Baxley, Sarah E ^a   Jiang, Wen ^a   Serra, Rosa ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Connexin; Lactation; Mammary glands; Oxytocin; Transgenic knockout model; WNT

Indexed keywords

CONNEXIN 43; OXYTOCIN; SERINE; WNT5A PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL COMMUNICATION; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; LACTATION; MAMMARY GLAND; MILK EJECTION; MOUSE; MOUSE MAMMARY TUMOR ONCOVIRUS; MYOEPITHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN PHOSPHORYLATION;

ANIMALS; CELL LINE; CONNEXIN 43; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION; LACTATION; MAMMARY GLANDS, ANIMAL; MICE; MICE, TRANSGENIC; MILK EJECTION; MODELS, ANIMAL; OXYTOCIN; PARTURITION; PHOSPHORYLATION; WNT PROTEINS;

MOUSE MAMMARY TUMOR VIRUS; MUS; MUS MUSCULUS;

EID: 81055126930     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.091645     Document Type: Article

References (38)

1. Richert MM, Schwertfeger KL, Ryder JW, Anderson SM. An atlas of mouse mammary gland development. J Mammary Gland Biol Neoplasia 2000; 5:227-241.
2. Peaker M. The mammary gland in mammalian evolution: a brief commentary on some of the concepts. J Mammary Gland Biol Neoplasia 2002; 7:347-353.
3. Brisken C, Rajaram RD. Alveolar and lactogenic differentiation. J Mammary Gland Biol Neoplasia 2006; 11:239-248.
4. Plante I, Laird DW. Decreased levels of connexin43 result in impaired development of the mammary gland in a mouse model of oculodentodigital dysplasia. Dev Biol 2008; 318:312-322.
5. Plante I, Wallis A, Shao Q, Laird DW. Milk secretion and ejection are impaired in the mammary gland of mice harboring a Cx43 mutant while expression and localization of tight and adherens junction proteins remain unchanged. Biol Reprod 2010; 82:837-847.
6. Bry C, Maass K, Miyoshi K, Willecke K, Ott T, Robinson GW, Hennighausen L. Loss of connexin 26 in mammary epithelium during early but not during late pregnancy results in unscheduled apoptosis and impaired development. Dev Biol 2004; 267:418-429.
7. Nakano H, Furuya K, Furuya S, Yamagishi S. Involvement of P2-purinergic receptors in intracellular Ca2+ responses and the contraction of mammary myoepithelial cells. Pflugers Arch 1997; 435:1-8.
8. Widelitz R. Wnt signaling through canonical and non-canonical pathways: recent progress. Growth Factors 2005; 23:111-116.
9. Kikuchi A, Kishida S, Yamamoto H. Regulation of Wnt signaling by protein-protein interaction and post-translational modifications. Exp Mol Med 2006; 38:1-10.
10. Kuhl M, Sheldahl LC, Park M, Miller JR, Moon RT. The Wnt/Ca2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet 2000; 16:279-283.
11. Veeman MT, Axelrod JD, Moon RT. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell 2003; 5:367-377.
12. Grigoryan T, Wend P, Klaus A, Birchmeier W. Deciphering the function of canonical Wnt signals in development and disease: conditional loss-and gain-of-function mutations of beta-catenin in mice. Genes Dev 2008; 22:2308-2341.
13. Gavin BJ, McMahon AP. Differential regulation of the Wnt gene family during pregnancy and lactation suggests a role in postnatal development of the mammary gland. Mol Cell Biol 1992; 12:2418-2423.
14. Roarty K, Serra R. Wnt5a is required for proper mammary gland development and TGF-beta-mediated inhibition of ductal growth. Development 2007; 134: 3929-3939.
15. Roarty K, Baxley SE, Crowley MR, Frost AR, Serra R. Loss of TGF-beta or Wnt5a results in an increase in Wnt/beta-catenin activity and redirects mammary tumour phenotype. Breast Cancer Res 2009; 11:R19.
16. Campeau E, Ruhl VE, Rodier F, Smith CL, Rahmberg BL, Fuss JO, Campisi J, Yaswen P, Cooper PK, Kaufman PD. A versatile viral system for expression and depletion of proteins in mammalian cells. PLoS One 2009; 4:e6529.
17. Tiscornia G, Singer O, Verma IM. Production and purification of lentiviral vectors. Nat Protoc 2006; 1:241-245.
18. Trosko JE, Chang CC, Wilson MR, Upham B, Hayashi T, Wade M. Gap junctions and the regulation of cellular functions of stem cells during development and differentiation. Methods 2000; 20:245-264.
19. Clark CC, Cohen I, Eichstetter I, Cannizzaro LA, McPherson JD, Wasmuth JJ, Iozzo RV. Molecular cloning of the human proto-oncogene Wnt-5A and mapping of the gene (WNT5A) to chromosome 3p14-p21. Genomics 1993; 18:249-260.
20. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992; 119:493-501.
21. Tong D, Lu X, Wang HX, Plante I, Lui E, Laird DW, Bai D, Kidder GM. A dominant loss-of-function GJA1 (Cx43) mutant impairs parturition in the mouse. Biol Reprod 2009; 80:1099-1106.
22. Solan JL, Lampe PD. Connexin43 phosphorylation: structural changes and biological effects. Biochem J 2009; 419:261-272.
23. Rakib MA, Kim YS, Jang WJ, Choi BD, Kim JO, Kong IK, Ha YL. Attenuation of 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced gap junctional intercellular communication (GJIC) inhibition in MCF-10A cells by c9,t11-conjugated linoleic acid. J Agric Food Chem 2010; 58:12022-12030.
24. McLachlan E, Shao Q, Wang HL, Langlois S, Laird DW. Connexins act as tumor suppressors in three-dimensional mammary cell organoids by regulating differentiation and angiogenesis. Cancer Res 2006; 66:9886-9894.
25. Uvnas-Moberg K, Eriksson M. Breastfeeding: physiological, endocrine and behavioural adaptations caused by oxytocin and local neurogenic activity in the nipple and mammary gland. Acta Paediatr 1996; 85:525-530.
26. Nishimori K, Young LJ, Guo Q, Wang Z, Insel TR, Matzuk MM. Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proc Natl Acad Sci U S A 1996; 93:11699-11704.
27. Young WS III, Shepard E, Amico J, Hennighausen L, Wagner KU, LaMarca ME, McKinney C, Ginns EI. Deficiency in mouse oxytocin prevents milk ejection, but not fertility or parturition. J Neuroendocrinol 1996; 8:847-853.
28. Takayanagi Y, Yoshida M, Bielsky IF, Ross HE, Kawamata M, Onaka T, Yanagisawa T, Kimura T, Matzuk MM, Young LJ, Nishimori K. Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc Natl Acad Sci U S A 2005; 102:16096-16101.
29. Reversi A, Cassoni P, Chini B. Oxytocin receptor signaling in myoepithelial and cancer cells. J Mammary Gland Biol Neoplasia 2005; 10:221-229.
30. Marozkina NV, Stiefel SM, Frierson HF Jr, Parsons SJ. MMTV-EGF receptor transgene promotes preneoplastic conversion of multiple steroid hormone-responsive tissues. J Cell Biochem 2008; 103:2010-2018.
31. Strizzi L, Bianco C, Hirota M, Watanabe K, Mancino M, Hamada S, Raafat A, Lawson S, Ebert AD, D'Antonio A, Losito S, Normanno N, Salomon DS. Development of leiomyosarcoma of the uterus in MMTV-CR-1 transgenic mice. J Pathol 2007; 211:36-44.
32. Bruzzone S, Franco L, Guida L, Zocchi E, Contini P, Bisso A, Usai C, De Flora A. A self-restricted CD38-connexin 43 cross-talk affects NAD+ and cyclic ADP-ribose metabolism and regulates intracellular calcium in 3T3 fibroblasts. J Biol Chem 2001; 276:48300-48308.
33. Yi FX, Boeldt DS, Gifford SM, Sullivan JA, Grummer MA, Magness RR, Bird IM. Pregnancy enhances sustained Ca2+ bursts and endothelial nitric oxide synthase activation in ovine uterine artery endothelial cells through increased connexin 43 function. Biol Reprod 2010; 82:66-75.
34. Song D, Liu X, Liu R, Yang L, Zuo J, Liu W. Connexin 43 hemichannel regulates H9c2 cell proliferation by modulating intracellular ATP and [Ca2+]. Acta Biochim Biophys Sin (Shanghai) 2010; 42:472-482.
35. Cotrina ML, Lin JH, Alves-Rodrigues A, Liu S, Li J, Azmi-Ghadimi H, Kang J, Naus CC, Nedergaard M. Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci U S A 1998; 95:15735-15740.
36. Laird DW, Yancey SB, Bugga L, Revel JP. Connexin expression and gap junction communication compartments in the developing mouse limb. Dev Dyn 1992; 195:153-161.
37. Yamaguchi TP, Bradley A, McMahon AP, Jones S. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 1999; 126:1211-1223.
38. Lo CW, Cohen MF, Huang GY, Lazatin BO, Patel N, Sullivan R, Pauken C, Park SM. Cx43 gap junction gene expression and gap junctional communication in mouse neural crest cells. Dev Genet 1997; 20:119-132.