Estrogen deficiency inhibits the odonto/osteogenic differentiation of dental pulp stem cells via activation of the NF-κB pathway

Cell and Tissue Research

Volumn 352, Issue 3, 2013, Pages 551-559

  Wang, Yanping ^a   Yan, Ming ^a   Yu, Yan ^a   Wu, Jintao ^a   Yu, Jinhua ^a   Fan, Zhipeng ^b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

Dental pulp; Differentiation; Estrogen; Nuclear factor kappa B; Rat (Sprague Dawley, female); Stem cell

Indexed keywords

4 (2 AMINOETHYLAMINO) 1,8 DIMETHYLIMIDAZO[1,2 A]QUINOXALINE; ALKALINE PHOSPHATASE; ESTROGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CONTROLLED STUDY; DENTAL PULP STEM CELL; DOWN REGULATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESTROGEN DEFICIENCY; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; INCISOR; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARIECTOMY; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELL; TOOTH PULP; UPREGULATION; WESTERN BLOTTING;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; DENTAL PULP; ESTROGENS; FEMALE; NF-KAPPA B; ODONTOGENESIS; OSTEOGENESIS; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; STEM CELLS;

RATTUS;

EID: 84878546262     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-013-1604-z     Document Type: Article

References (42)

1. Alles N, Soysa NS, Hayashi J, Khan M, Shimoda A, Shimokawa H, Ritzeler O, Akiyoshi K, Aoki K, Ohya K (2010) Suppression of NF-kappaB increases bone formation and ameliorates osteopenia in ovariectomized mice. Endocrinology 151:4626-4634
2. Cao M, Shu L, Li J, Su J, Zhang W, Wang Q, Guo T, Ding Y (2007) The expression of estrogen receptors and the effects of estrogen on human periodontal ligament cells. Methods Find Exp Clin Pharmacol 29:329-335
3. Celil AB, Hollinger JO, Campbell PG (2005) Osx transcriptional regulation is mediated by additional pathways to BMP2/Smad signaling. J Cell Biochem 95:518-528
4. Chen S, Gluhak-Heinrich J, Wang YH, Wu YM, Chuang HH, Chen L, Yuan GH, Dong J, Gay I, MacDougall M (2009) Runx2, osx, and dspp in tooth development. J Dent Res 88:904-909
5. d'Aquino R, Graziano A, Sampaolesi M, Laino G, Pirozzi G, De Rosa A, Papaccio G (2007) Human postnatal dental pulp cells co-differentiate into osteoblasts and endotheliocytes: a pivotal synergy leading to adult bone tissue formation. Cell Death Differ 14:1162-1171
6. d'Aquino R, De Rosa A, Laino G, Caruso F, Guida L, Rullo R, Checchi V, Laino L, Tirino V, Papaccio G (2009a) Human dental pulp stem cells: from biology to clinical applications. J Exp Zool B Mol Dev Evol 312B:408-415
7. d'Aquino R, De Rosa A, Lanza V, Tirino V, Laino L, Graziano A, Desiderio V, Laino G, Papaccio G (2009b) Human mandible bone defect repair by the grafting of dental pulp stem/progenitor cells and collagen sponge biocomplexes. Eur Cell Mater 18:75-83
8. Demarco FF, Casagrande L, Zhang Z, Dong Z, Tarquinio SB, Zeitlin BD, Shi S, Smith AJ, Nor JE (2010) Effects of morphogen and scaffold porogen on the differentiation of dental pulp stem cells. J Endod 36:1805-1811
9. Dvorak G, Reich K, Tangl S, Lill CA, Gottschalk-Baron M, Watzek G, Gruber R, Haas R (2009) Periodontal histomorphometry and status of aged sheep subjected to ovariectomy, malnutrition and glucocorticoid application. Arch Oral Biol 54:857-863
10. Fahey JV, Wright JA, Shen L, Smith JM, Ghosh M, Rossoll RM, Wira CR (2008) Estradiol selectively regulates innate immune function by polarized human uterine epithelial cells in culture. Mucosal Immunol 1:317-325
11. Franke S, Ruster C, Pester J, Hofmann G, Oelzner P, Wolf G (2011) Advanced glycation end products affect growth and function of osteoblasts. Clin Exp Rheumatol 29:650-660
12. Giannoni E, Guignard L, Knaup Reymond M, Perreau M, Roth-Kleiner M, Calandra T, Roger T (2011) Estradiol and progesterone strongly inhibit the innate immune response of mononuclear cells in newborns. Infect Immun 79:2690-2698
13. Graziano A, d'Aquino R, Laino G, Papaccio G (2008) Dental pulp stem cells: a promising tool for bone regeneration. Stem Cell Rev 4:21-26
14. Iejima D, Sumita Y, Kagami H, Ando Y, Ueda M (2007) Odontoblast marker gene expression is enhanced by a CC-chemokine family protein MIP-3alpha in human mesenchymal stem cells. Arch Oral Biol 52:924-931
15. Johnson RB, Gilbert JA, Cooper RC, Dai X, Newton BI, Tracy RR, West WF, DeMoss TL, Myers PJ, Streckfus CF (1997) Alveolar bone loss one year following ovariectomy in sheep. J Periodontol 68:864-871
16. Kanda N, Watanabe S (2003) 17Beta-estradiol inhibits the production of RANTES in human keratinocytes. J Invest Dermatol 120:420-427
17. Kawamoto S, Ejiri S, Nagaoka E, Ozawa H (2002) Effects of oestrogen deficiency on osteoclastogenesis in the rat periodontium. Arch Oral Biol 47:67-73
18. Khosla S, Melton LJ 3rd, Riggs BL (2011) The unitary model for estrogen deficiency and the pathogenesis of osteoporosis: is a revision needed? J Bone Miner Res 26:441-451
19. Komori T (2010) Regulation of osteoblast differentiation by Runx2. Adv Exp Med Biol 658:43-49
20. Laino G, d'Aquino R, Graziano A, Lanza V, Carinci F, Naro F, Pirozzi G, Papaccio G (2005) A new population of human adult dental pulp stem cells: a useful source of living autologous fibrous bone tissue (LAB). J Bone Miner Res 20:1394-1402
21. Lee SS, Sharma AR, Choi BS, Jung JS, Chang JD, Park S, Salvati EA, Purdue EP, Song DK, Nam JS (2012) The effect of TNFalpha secreted from macrophages activated by titanium particles on osteogenic activity regulated by WNT/BMP signaling in osteoprogenitor cells. Biomaterials 33:4251-4263
22. Ma D, Ma Z, Zhang X, Wang W, Yang Z, Zhang M, Wu G, Lu W, Deng Z, Jin Y (2009) Effect of age and extrinsic microenvironment on the proliferation and osteogenic differentiation of rat dental pulp stem cells in vitro. J Endod 35:1546-1553
23. Mamalis A, Markopoulou C, Lagou A, Vrotsos I (2011) Oestrogen regulates proliferation, osteoblastic differentiation, collagen synthesis and periostin gene expression in human periodontal ligament cells through oestrogen receptor beta. Arch Oral Biol 56:446-455
24. Moriya Y, Ito K, Murai S (1998) Effects of experimental osteoporosis on alveolar bone loss in rats. J Oral Sci 40:171-175
25. Muhammad N, Luke DA, Shuid AN, Mohamed N, Soelaiman IN (2012) Two different isomers of vitamin E prevent bone loss in postmenopausal osteoporosis rat model. Evid Based Complement Alternat Med: eCAM 2012:161527
26. Ni P, Fu S, Fan M, Guo G, Shi S, Peng J, Luo F, Qian Z (2011) Preparation of poly(ethylene glycol)/polylactide hybrid fibrous scaffolds for bone tissue engineering. Int J Nanomed 6:3065-3075
27. Takahashi T (2011) Overexpression of Runx2 and MKP-1 stimulates transdifferentiation of 3T3-L1 preadipocytes into bone-forming osteoblasts in vitro. Calcif Tissue Int 88:336-347
28. Tang Y, Xie H, Chen J, Geng L, Chen H, Li X, Hou Y, Lu L, Shi S, Zeng X, Sun L (2013) Activated NF-kappaB in bone marrow mesenchymal stem cells from systemic lupus erythematosus patients inhibits osteogenic differentiation through downregulating Smad signaling. Stem Cells Dev 22:668-678
29. Wade-Gueye NM, Boudiffa M, Vanden-Bossche A, Laroche N, Aubin JE, Vico L, Lafage-Proust MH, Malaval L (2012) Absence of bone sialoprotein (BSP) impairs primary bone formation and resorption: the marrow ablation model under PTH challenge. Bone 50:1064-1073
30. Wang S, Mu J, Fan Z, Yu Y, Yan M, Lei G, Tang C, Wang Z, Zheng Y, Yu J, Zhang G (2012) Insulin-like growth factor 1 can promote the osteogenic differentiation and osteogenesis of stem cells from apical papilla. Stem Cell Res 8:346-356
31. Wang YX, Ma ZF, Huo N, Tang L, Han C, Duan YZ, Jin Y (2011) Porcine tooth germ cell conditioned medium can induce odontogenic differentiation of human dental pulp stem cells. J Tissue Eng Regen Med 5:354-362
32. Wattanaroonwong N, Schoenmaker T, Vries TJ de, Everts V (2011) Oestrogen inhibits osteoclast formation induced by periodontal ligament fibroblasts. Arch Oral Biol 56:212-219
33. Xu J, Wu HF, Ang ES, Yip K, Woloszyn M, Zheng MH, Tan RX (2009) NF-kappaB modulators in osteolytic bone diseases. Cytokine Growth Factor Rev 20:7-17
34. Yamaguchi M, Arbiser JL, Weitzmann MN (2011) Honokiol stimulates osteoblastogenesis by suppressing NF-kappaB activation. Int J Mol Med 28:1049-1053
35. Yan M, Yu Y, Zhang G, Tang C, Yu J (2011) A journey from dental pulp stem cells to a bio-tooth. Stem Cell Rev 7:161-171
36. Yang X, Zhang S, Pang X, Fan M (2012) Pro-inflammatory cytokines induce odontogenic differentiation of dental pulp-derived stem cells. J Cell Biochem 113:669-677
37. Yu J, He H, Tang C, Zhang G, Li Y, Wang R, Shi J, Jin Y (2010) Differentiation potential of STRO-1+ dental pulp stem cells changes during cell passaging. BMC Cell Biol 11:32
38. Yu Y, Mu J, Fan Z, Lei G, Yan M, Wang S, Tang C, Wang Z, Yu J, Zhang G (2012) Insulin-like growth factor 1 enhances the proliferation and osteogenic differentiation of human periodontal ligament stem cells via ERK and JNK MAPK pathways. Histochem Cell Biol 137:513-525
39. Zhang B, Li Y, Zhou Q, Ding Y (2011a) Estrogen deficiency leads to impaired osteogenic differentiation of periodontal ligament stem cells in rats. Tohoku J Exp Med 223:177-186
40. Zhang J, Tu Q, Grosschedl R, Kim MS, Griffin T, Drissi H, Yang P, Chen J (2011b) Roles of SATB2 in osteogenic differentiation and bone regeneration. Tissue Eng Part A 17:1767-1776
41. Zhang M, Chen FM, Wang AH, Chen YJ, Lv X, Wu S, Zhao RN (2012) Estrogen and its receptor enhance mechanobiological effects in compressed bone mesenchymal stem cells. Cells Tissues Organs 195:400-413
42. Zhao JW, Gao ZL, Mei H, Li YL, Wang Y (2011) Differentiation of human mesenchymal stem cells: the potential mechanism for estrogen-induced preferential osteoblast versus adipocyte differentiation. Am J Med Sci 341:460-468