Serotonin regulates calcium homeostasis in lactation by epigenetic activation of hedgehog signaling

Molecular Endocrinology

Volumn 28, Issue 11, 2014, Pages 1866-1874

  Laporta, Jimena ^a   Keil, Kimberly P ^b   Weaver, Samantha R ^a   Cronick, Callyssa M ^a   Prichard, Austin P ^a   Crenshaw, Thomas D ^a   Heyne, Galen W ^b   Vezina, Chad M ^b   Lipinski, Robert J ^b   Hernandez, Laura L ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYTRYPTOPHAN; CALCIUM; PARATHYROID HORMONE RELATED PROTEIN; SEROTONIN; SONIC HEDGEHOG PROTEIN; TRYPTOPHAN HYDROXYLASE; SHH PROTEIN, MOUSE; TPH1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREAST; CALCIUM BLOOD LEVEL; CALCIUM BONE LEVEL; CALCIUM HOMEOSTASIS; CALCIUM MOBILIZATION; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; EPIGENETICS; FEMALE; FIBROBLAST; GENE; GENE ACTIVATION; GENE CONTROL; GENE INACTIVATION; GENE LOCUS; IN VITRO STUDY; IN VIVO STUDY; LACTATION; MAMMARY GLAND; MOLECULAR MECHANICS; MOUSE; MOUSE MODEL; NONHUMAN; OSTEOCLAST ACTIVITY; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SHH GENE; SIGNAL TRANSDUCTION; THIRD TRIMESTER PREGNANCY; TRANSCRIPTION INITIATION SITE; ANIMAL; C57BL MOUSE; GENETIC EPIGENESIS; GENETICS; HOMEOSTASIS; METABOLISM; OSTEOCLAST; PREGNANCY; PROMOTER REGION; UDDER;

ANIMALS; CALCIUM; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; FIBROBLASTS; HEDGEHOG PROTEINS; HOMEOSTASIS; LACTATION; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED C57BL; OSTEOCLASTS; PARATHYROID HORMONE-RELATED PROTEIN; PREGNANCY; PROMOTER REGIONS, GENETIC; SEROTONIN; SIGNAL TRANSDUCTION; TRYPTOPHAN HYDROXYLASE;

EID: 84908351861     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2014-1204     Document Type: Article

References (42)

1. Kovacs CS, Kronenberg HM. Maternal-fetal calcium and bone metabolism during pregnancy, puerperium, and lactation. Endocr Rev. 1997;18(6):832–872.
2. Wysolmerski JJ. Interactions between breast, bone, and brain regulate mineral and skeletal metabolism during lactation. In: Zaidi M, ed. Skeletal Biology and Medicine. Vol 11922010:161–169. Ann NY Acad Sci. 2010;1192:161–169.
3. Goff JP. The monitoring, prevention, and treatment of milk fever and subclinical hypocalcemia in dairy cows. Vet J. 2008;176(1): 50–57.
4. Reinhardt TA, Lippolis JD, McCluskey BJ, Goff JP, Horst RL. Prevalence of subclinical hypocalcemia in dairy herds. Vet J. 2011; 188(1):122–124.
5. Davidson AP. Reproductive causes of hypocalcemia. Top Companion Anim Med. 2012;27(4):165–166.
6. Matsuda M, Imaoka T, Vomachka AJ, et al. Serotonin regulates mammary gland development via an autocrine-paracrine loop. Dev Cell. 2004;6(2):193–203.
7. Hannon J, Hoyer D. Molecular biology of 5-HT receptors. Behav Brain Res. 2008;195(1):198–213.
8. Collier RJ, Hemandez LL, Horseman ND. Serotonin as a homeo-static regulator of lactation. Domest Anim Endocrinol. 2012;43(2): 161–170.
9. Hernandez LL, Collier JL, Vomachka AJ, Collier RJ, Horseman ND. Suppression of lactation and acceleration of involution in the bovine mammary gland by a selective serotonin reuptake inhibitor. J Endocrinol. 2011;209(1):45–54.
10. Hernandez LL, Stiening CM, Wheelock JB, Baumgard LH, Parkhurst AM, Collier RJ. Evaluation of serotonin as a feedback inhibitor of lactation in the bovine. J Dairy Sci. 2008;91(5):1834–1844.
11. Pai VP, Horseman ND. Biphasic regulation of mammary epithelial resistance by serotonin through activation of multiple pathways. J Biol Chem. 2008;283(45):30901–30910.
12. Laporta J, Peters TL, Weaver SR, Merriman KE, Hernandez LL. Feeding 5-hydroxy-L-tryptophan during the transition from pregnancy to lactation increases calcium mobilization from bone in rats. Domest Anim Endocrinol. 2013;44(4):176–184.
13. Hernandez LL, Gregerson KA, Horseman ND. Mammary gland serotonin regulates parathyroid hormone-related protein and other bone-related signals. Am J Physiol Endocrinol Metab. 2012;302(8): E1009–E1015.
14. Kovacs CS. Calcium and bone metabolism disorders during pregnancy and lactation. Endocrinol Metab Clin North Am. 2011; 40(4):795–826.
15. Mamillapalli R, VanHouten J, Dann P, et al. Mammary-specific ablation of the calcium-sensing receptor during lactation alters maternal calcium metabolism, milk calcium transport, and neonatal calcium accrual. Endocrinology. 2013;154(9):3031–3042.
16. Sterling JA, Oyajobi BO, Grubbs B, et al. The hedgehog signaling molecule Gli2 induces parathyroid hormone-related peptide expression and osteolysis in metastatic human breast cancer cells. Cancer Res. 2006;66(15):7548-7553.
17. Katoh Y, Katoh M. Hedgehog target genes: mechanisms of carcinogenesis induced by aberrant hedgehog signaling activation. Curr MolMed. 2009;9(7):873-886.
18. Jemtland R, Divieti P, Lee K, Segre GV. Hedgehog promotes primary osteoblast differentiation and increases PTHrP mRNA expression and iPTHrP secretion. Bone. 2003;32(6):611-620.
19. Lipinski RJ, Gipp JJ, Zhang JX, Doles JD, Bushman W. Unique and complimentary activities of the Gli transcription factors in Hedgehog signaling. Exp Cell Res. 2006;312(11):1925-1938.
20. Tavella S, Biticchi R, Schito A, et al. Targeted expression of SHH affects chondrocyte differentiation, growth plate organization, and Sox9 expression. J Bone Miner Res. 2004;19(10):1678-1688.
21. Holtje M, Winter S, Walther D, et al. The vesicular monoamine content regulates VMAT2 activity through Ga(q) mouse platelets—evidence for autoregulation of vesicular transmitter uptake. J Biol Chem. 2003;278(18):15850-15858.
22. Chabbi-Achengli Y, Coudert AE, Callebert J, et al. Decreased oste-oclastogenesis in serotonin-deficient mice. Proc Natl Acad Sci USA. 2012;109(7):2567-2572.
23. Keil KP, Abler LL, Mehta V, et al. DNA methylation of E-cadherin is a priming mechanism for prostate development. Dev Biol. 2014; 3(14):00048-00047.
24. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-SSC) method. Methods. 2001;25(4):402-408.
25. Lipinski RJ, Bijlsma MF, Gipp JJ, Podhaizer DJ, Bushman W. Establishment and characterization of immortalized Gli-null mouse embryonic fibroblast cell lines. BMC Cell Biol. 2008;9:49.
26. Lamp EC, Drexler HG. Biology of tartrate-resistant acid phosphatase. Leukemia Lymphoma. 2000;39(5-6):477-484.
27. Kitazawa S, Kitazawa R, Tamada H, Maeda S. Promoter structure of human sonic hedgehog gene. Biochim Biophys Acta Gene Struct Express. 1998;1443(3):358-363.
28. Wysolmerski JJ. Parathyroid hormone-related protein: an update. J Clin Endocrinol Metab. 2012;97(9):2947-2956.
29. Michno K, Boras-Granic K, Mill P, Hui CC, Hamel PA. Shh expression is required for embryonic hair follicle but not mammary gland development. Dev Biol. 2003;264(1):153-165.
30. Veltmaat JM, Relaix F, Kratochwil K, et al. Gli3-mediated somitic Fgf10 expression gradients are required for the induction and patterning of mammary epithelium along the embryonic axes. Development. 2006;133(12):2325–2335.
31. Lewis MT, Ross S, Strickland PA, et al. The Gli2 transcription factor is required for normal mouse mammary gland development. Dev Biol. 2001;238(1):133–144.
32. Goodrich LV, MilenkovicL,Higgins KM, Scott MP. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science. 1997;277(5329):1109–1113.
33. Geng X, Speirs C, Lagutin O, Inbal A, et al. Haploinsufficiency of Six3 fails to activate sonic hedgehog expression in the ventral fore-brain and causes holoprosencephaly. Dev Cell. 2008;15(2):236–247.
34. Ten Haaf A, Franken L, Heymann C, et al. Paradox of sonic hedgehog (SHH) transcriptional regulation: alternative transcription initiation overrides the effect of downstream promoter DNA methyl-ation. Epigenetics. 2011;6(4):466–478.
35. Tsukiji N, Amano T, Shiroishi T. A novel regulatory element for Shh expression in the lung and gut of mouse embryos. Mech Dev. 2014;131:127–136.
36. Shuey DL, Sadler TW, Lauder JM. Serotonin as a regulator of craniofacial morphogenesis—site specific malformations following exposure to serotonin uptake inhibitors. Teratology. 1992;46(4): 367–378.
37. Reisoli E, De Lucchini S, Nardi I, Ori M. Serotonin 2B receptor signaling is required for craniofacial morphogenesis and jaw joint formation in Xenopus. Development. 2010;137(17):2927–2937.
38. Lipinski RJ, Song C, Sulik KK, et al. Cleft lip and palate results from hedgehog signaling antagonism in the mouse: phenotypic characterization and clinical implications. Birth Defects Res Part A Clin Mol Teratol. 2010;88(4):232–240.
39. Das S, Tucker JA, Khullar S, Samant RS, Shevde LA. Hedgehog signaling in tumor cells facilitates osteoblast-enhanced osteolytic metastases. Plos One. 2012;7(3):e34374.
40. Eom C-S, Lee H-K, Ye S, Park SM, Cho K-H. Use of selective serotonin reuptake inhibitors and risk of fracture: a systematic review and meta-analysis. J Bone Miner Res. 2012;27(5):1186–1195.
41. Shea MLO, Garfield LD, Teitelbaum S, et al. Serotonin-norepi-nephrine reuptake inhibitor therapy in late-life depression is associated with increased marker of bone resorption. Osteoporos Int. 2013;24(5):1741–1749.
42. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol (Clifton, NJ). 2000; 132:365–386.