Crucial role of Notch signaling in osteogenic differentiation of periodontal ligament stem cells in osteoporotic rats

Cell Biology International

Volumn 38, Issue 6, 2014, Pages 729-736

  Li, Ying ^a   Li, S Q ^b   Gao, Y M ^c   Li, Jin ^d   Zhang, Bin ^c  

^a AIR FORCE GENERAL HOSPITAL   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c CHINESE PLA GENERAL HOSPITAL   (China)

^d GENERAL HOSPITAL OF CHINESE PEOPLE'S ARMED POLICE FORCES   (China)

Author keywords

Notch signaling; Ofsteoporosis; Osteogenic differentiation; Periodontal ligament stem cells

Indexed keywords

CALCIUM; GAMMA SECRETASE INHIBITOR; JAGGED1; MESSENGER RNA; NOTCH RECEPTOR; NOTCH1 RECEPTOR; CALCIUM BINDING PROTEIN; MEMBRANE PROTEIN; NOTCH1 PROTEIN, RAT; SECRETASE; SERRATE PROTEINS; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; CELL DIFFERENTIATION; CELL ISOLATION; CULTURE MEDIUM; FEMALE; GENE EXPRESSION; NONHUMAN; OSTEOPENIA; OSTEOPOROSIS; OVARIECTOMY; PERIODONTAL LIGAMENT; PERIODONTAL LIGAMENT STEM CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SHAM PROCEDURE; SIGNAL TRANSDUCTION; STEM CELL; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CYTOLOGY; FEMUR; GENETICS; METABOLISM; MOLAR TOOTH; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CALCIUM; CALCIUM-BINDING PROTEINS; FEMALE; FEMUR; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MOLAR; OSTEOGENESIS; OSTEOPOROSIS; OVARIECTOMY; PERIODONTAL LIGAMENT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, NOTCH1; RNA, MESSENGER; SIGNAL TRANSDUCTION; STEM CELLS; UP-REGULATION;

EID: 84900821470     PISSN: 10656995     EISSN: 10958355     Source Type: Journal    
DOI: 10.1002/cbin.10257     Document Type: Article

References (44)

1. Bartold P, Mcculloch CAG, Narayanan AS, Pitaru S (2003) Tissue engineering: a new paradigm for periodontal regeneration based on molecular and cell biology. Periodontology 2000. 24: 253-69.
2. Braniste V, Jouault A, Gaultier E, Polizzi A, Buisson-Brenac C, Leveque M, Martin P, Theodorou V, Fioramonti J, Houdeau E (2010) Impact of oral bisphenol a at reference doses on intestinal barrier function and sex differences after perinatal exposure in rats. Proc Natl Acad Sci 107: 448-53.
3. Bray SJ (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7: 678-89.
4. Chan A, van Bezooijen RL, Löwik C (2007) Anew paradigm in the treatment of osteoporosis: Wnt pathway proteins and their antagonists.. Curr Opin Invest Drugs (London, England: 2000) 8: 293.
5. Chen S, Marino V, Gronthos S, Bartold PM (2006) Location of putative stem cells in human periodontal ligament. J Periodontal Res 41: 547-53.
6. Dvornyk V, Recker R, Deng HW (2003) Gene expression studies of osteoporosis: implications for microarray research. Osteoporosis Int 14: 451-61.
7. Engin F, Yao Z, Yang T, Zhou G, Bertin T, JiangMMet al. (2008) Dimorphic effects of Notch signaling in bone homeostasis. Nat Med 14: 299-305.
8. Gay IC, Chen S, MacDougall M (2007) Isolation and characterization of multipotent human periodontal ligament stem cells. Orthod Craniofac Res 10: 149-60.
9. Gronthos S, Mrozik K, Shi S, Bartold PM (2006) Ovine periodontal ligament stem cells: isolation, characterization, and differentiation potential. Calcif Tissue Int 79: 310-7.
10. Hajdu M, Luttun A, Pelacho B, Burns TC, Chase L, Gutiérrez- Pérez M et al. (2007) Transcriptional characterization of the Notch signaling pathway in rodent multipotent adult progenitor cells. Pathol Oncol Res 13: 302-10.
11. He F, Yang Z, Tan Y, Yu N, Wang X, Yao N et al. (2009) Effects of Notch ligand Delta1 on the proliferation and differentiation of human dental pulp stem cells in vitro. Arch Oral Biol 54: 216-22.
12. Hilton MJ, Tu X, Wu X, Bai S, Zhao H, Kobayashi T et al. (2008) Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation. Nat Med 14: 306-14.
13. Huang QY, Recker RR, Deng HW (2003) Searching for osteoporosis genes in the post-genome era: progress and challenges. Osteoporo Int 14: 701-15.
14. Hurlbut GD, Kankel MW, Lake RJ, Artavanis-Tsakonas S (2007) Crossing paths with Notch in the hyper-network. Curr Opin Cell Biol 19: 166-75.
15. Jing D, Shen G, Huang J, Xie K, Cai J, Xu Q et al. (2010) Circadian rhythm affects the preventive role of pulsed electromagnetic fields on ovariectomy-induced osteoporosis in rats. Bone 46: 487-95.
16. Köhler C, Bell AW, Bowen WC, Monga SP, Fleig W, Michalopoulos GK (2004) Expression of Notch-1 and its ligand Jagged-1 in rat liver during liver regeneration. Hepatology 39: 1056-65.
17. Kaneda T, Miyauchi M, Takekoshi T, Kitagawa S, Kitagawa M, Shiba H et al. (2006) Characteristics of periodontal ligament subpopulations obtained by sequential enzymatic digestion of rat molar periodontal ligament. Bone 38: 420-6.
18. Kemoun P, Laurencin-Dalicieux S, Rue J, Vaysse F, Romeas A, Arzate H et al. (2007) Localization of STRO-1, BMP-2/-3/-7, BMP receptors and phosphorylated Smad-1 during the formation of mouse periodontium. Tissue Cell 39: 257-66.
19. Kimmel D, Moran E, Bogoch E (1999) Animal models of osteopenia or osteoporosis. Animal Models in Orthopaedic Research. Boca Raton, FL, USA: CRC Press, pp. 280-305.
20. Kopan R, Ilagan MXG (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137: 216-33.
21. Lane NE, Haupt D, Kimmel DB, Modin G, Kinney JH (1999) Early estrogen replacement therapy reverses the rapid loss of trabecular bone volume and prevents further deterioration of connectivity in the rat. J Bone Miner Res 14: 206-14.
22. Liang L, Yu J, Wang Y, Wang G, Ding Y (2008) Effect of estrogen receptor beta on the osteoblastic differentiation function of human periodontal ligament cells. Arch Oral Biol 53: 553-7.
23. Ma XB, Jia XS, Liu YL, Wang LL, Sun SL, Song N et al. (2008) Expression and role of Notch signalling in the regeneration of rat tracheal epithelium. Cell Prolif 42: 15-28.
24. Mudda JA, Bajaj M (2011) Stem cell therapy: a challenge to periodontist. Indian J Dent Res 22: 132-9.
25. Niessen K, Karsan A (2008) Notch signaling in cardiac development. Circ Res 102: 1169-81.
26. Niu T, Xu X (2001) Candidate genes for osteoporosis: therapeutic implications. Am J PharmacoGenomics 1: 11-9.
27. Nobta M, Tsukazaki T, Shibata Y, Xin C, Moriishi T, Sakano S et al. (2005) Critical regulation of bone morphogenetic proteininduced osteoblastic differentiation by Delta1/Jagged1-activated Notch1 signaling. J Biol Chem 280: 15842-8.
28. Osathanon T, Subbalekha K, Sastravaha P, Pavasant P (2012) Notch signaling inhibits the adipogenic differentiation of single-cell-derived mesenchymal stem cell clones isolated from human adipose tissue. Cell Biol Int 36: 1161-70.
29. Pan F, Zhang R, Wang G, Ding Y (2011) Oestrogen receptors are involved in the osteogenic differentiation of periodontal ligament stem cells. Biosci Rep 31: 117-24.
30. Rizzoli R, Bonjour J, Ferrari S (2001) Osteoporosis genetics and hormones. J Mol Endocrinol 26: 79-94.
31. Sciaudone M, Gazzerro E, Priest L, Delany AM, Canalis E (2003) Notch 1 impairs osteoblastic cell differentiation. Endocrinology 144: 5631-9.
32. Seo BM, Miura M, Gronthos S, Mark Bartold P, Batouli S, Brahim J et al. (2004) Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364: 149-55.
33. Shawber CJ, Kitajewski J (2004) Notch function in the vasculature: insights from zebrafish, mouse and man. Bioessays 26: 225-34.
34. Shimono M, Ishikawa T, Ishikawa H, Matsuzaki H, Hashimoto S, Muramatsu T et al. (2003) Regulatory mechanisms of periodontal regeneration. Microsc Res Tech 60: 491-502.
35. Shindo K, Kawashima N, Sakamoto K, Yamaguchi A, Umezawa A, Takagi M et al. (2003) Osteogenic differentiation of the mesenchymal progenitor cells, Kusa is suppressed by Notch signaling. Exp Cell Res 290: 370-80.
36. Strait K, YAN L, Dillehay DL, Weitzmann MN (2008) Suppression of NF-KB activation blocks osteoclastic bone resorption during estrogen deficiency. Int J Mol Med 21: 521-5.
37. Tezuka KI, Yasuda M, Watanabe N, Morimura N, Kuroda K, Miyatani S et al. (2002) Stimulation of osteoblastic cell differentiation by Notch. J Bone Miner Res 17: 231-9.
38. Thanaphum O, Nunthawan N, Jeeranan M, Prasit P (2013) BFGF and JAGGED1 Regulate Alkaline Phosphatase Expression and Mineralization in Dental Tissue Derived Mesenchymal Stem Cells. J Cell Biochem 114: 2551-61.
39. Ugarte F, Ryser M, Thieme S, Fierro FA, Navratiel K, Bornhäuser M et al. (2009) Notch signaling enhances osteogenic differentiation while inhibiting adipogenesis in primary human bone marrow stromal cells. Exp Hematol 37: 867-75 e1 e1.
40. Wu J, Jin F, Tang L, Yu J, Xu L, Yang Z et al. (2008) Dentin noncollagenous proteins (dNCPs) can stimulate dental follicle cells to differentiate into cementoblast lineages. Biol Cell 100: 291-302.
41. Xu J, Wang W, Kapila Y, Lotz J, Kapila S (2009) Multiple differentiation capacity of STRO-1p/CD146p PDL mesenchymal progenitor cells. Stem Cells Dev 18: 487-96.
42. Zhang B, Li Y, Zhou Q, Ding Y (2011) Estrogen deficiency leads to impaired osteogenic differentiation of periodontal ligament stem cells in rats. Tohoku J Exp Med 223: 177-86.
43. Zhang C, Chang J, Sonoyama W, Shi S, Wang CY (2008) Inhibition of human dental pulp stem cell differentiation by Notch signaling. J Dent Res 87: 250-5.
44. Zheng W, Wang S, Ma D, Tang L, Duan Y, Jin Y (2009) Loss of proliferation and differentiation capacity of aged human periodontal ligament stem cells and rejuvenation by exposure to the young extrinsic environment. Tissue Eng, Part A 15: 2363-71.