Human dental pulp cells exhibit bone cell-like responsiveness to fluid shear stress

Cytotherapy

Volumn 13, Issue 2, 2011, Pages 214-226

  Kraft, David Christian Evar ^a   Bindslev, Dorth Arenholt ^a   Melsen, Birte ^a   Klein Nulend, Jenneke ^b  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Cell differentiation; Cyclooxygenase; Dental pulp; Human; Mechanical stress; Nitric oxide; Osteoblasts; Prostaglandin E2; Stem cells; Tissue engineering

Indexed keywords

CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; NITRIC OXIDE; PROSTAGLANDIN E2;

ANIMAL TISSUE; ARTICLE; BONE CELL; BONE DEVELOPMENT; CELL DIFFERENTIATION; CULTURE MEDIUM; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INCUBATION TIME; MINERALIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHEAR STRESS; TISSUE ENGINEERING; TOOTH PULP; UPREGULATION;

EID: 78751546013     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.3109/14653249.2010.487897     Document Type: Article

References (64)

1. Abdallah BM, Kassem M. Human mesenchymal stem cells: from basic biology to clinical applications. Gene Ther. 2008; 15:109-16.
2. Laino G, Graziano A, d A quino R, Pirozzi G, Lanza V, Valiante S,et al. An approachable human adult stem cell source for hard-tissue engineering. J Cell Physiol. 2006;206: 693-701.
3. Laino G, d A quino R, Graziano A, Lanza V, Carinci F, Naro F,et al. A new population of human adult dental pulp stem cells: a useful source of living autologous fi brous bone tissue (LAB). J Bone Miner Res. 2005;20:1394-402.
4. Zheng Y, Liu Y, Zhang CM, Zhang HY, Li WH, Shi S,et al. Stem cells from deciduous tooth repair mandibular defect in swine. J Dent Res. 2009;88:249-54.
5. Otaki S, Ueshima S, Shiraishi K, Sugiyama K, Hamada S, Yorimoto M,et al. Mesenchymal progenitor cells in adult human dental pulp and their ability to form bone when transplanted into immunocompromised mice. Cell Biol Int. 2007; 31:1191-7.
6. Batouli S, Miura M, Brahim J, Tsutsui TW, Fisher LW, Gronthos S,et al. Comparison of stem-cell-mediated osteogenesis and dentinogenesis. J Dent Res. 2003;82:976-81.
7. Zhang W, Walboomers XF, Shi S, Fan M, Jansen JA. Multilineage differentiation potential of stem cells derived from human dental pulp after cryopreservation. Tissue Eng. 2006; 12:2813-23.
8. Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA. 2000;97:13625-30.
9. d A quino R, Graziano A, Sampaolesi M, Laino G, Pirozzi G, De RA,et al. Human postnatal dental pulp cells co-differentiate into osteoblasts and endotheliocytes: a pivotal synergy leading to adult bone tissue formation. Cell Death Differ. 2007;14:1162-71.
10. Pierdomenico L, Bonsi L, Calvitti M, Rondelli D, Arpinati M, Chirumbolo G,et al. Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation. 2005;80:836-42.
11. Turner CH, Pavalko FM. Mechanotransduction and functional response of the skeleton to physical stress: the mechanisms and mechanics of bone adaptation. J Orthop Sci. 1998; 3:346-55.
12. Burger EH, Klein-Nulend J. Mechanotransduction in bone: role of the lacuno-canalicular network. FASEB J. 1999;13(Suppl): 101-12.
13. Burger EH, Klein-Nulend J, Smit TH. Strain-derived canalicular fl uid fl ow regulates osteoclast activity in a remodeling osteon: a proposal. J Biomech. 2003;36:1453-9.
14. Ajubi NE, Klein-Nulend J, Alblas MJ, Burger EH, Nijweide PJ. Signal transduction pathways involved in fl uid fl owinduced PGE2 production by cultured osteocytes. Am J Physiol. 1999;276:171-8.
15. Piekarski K, Munro M. Transport mechanism operating between blood supply and osteocytes in long bones. Nature. 1977;269:80-2.
16. Knothe Tate ML, Niederer P, Knothe U. In vivo tracer transport through the lacunocanalicular system of rat bone in an environment devoid of mechanical loading. Bone. 1998;22: 107-17.
17. Bacabac RG, Smit TH, Cowin SC, Van Loon JJWA, Nieuwstadt FT, Heethaar R,et al. Dynamic shear stress in parallelplate fl ow chambers. J Biomech. 2005;38:159-67.
18. Ke HZ, Shen VW, Qi H, Crawford DT, Wu DD, Liang XG,et al. Prostaglandin E2 increases bone strength in intact rats and in ovariectomized rats with established osteopenia. Bone. 1998;23:249-55.
19. Miller SC, Marks SC Jr. Local stimulation of new bone formation by prostaglandin E1: quantitative histomorphometry and comparison of delivery by minipumps and controlled-release pellets. Bone. 1993;14:143-51.
20. Klein-Nulend J, Semeins CM, Ajubi NE, Nijweide PJ, Burger EH. Pulsating fl uid fl ow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fi broblasts: correlation with prostaglandin upregulation. Biochem Biophys Res Commun. 1995;217:640-8.
21. Klein-Nulend J, Van der Plas A, Semeins CM, Ajubi NE, Frangos JA, Nijweide PJ,et al. Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J. 1995;9:441-5.
22. Paphangkorakit J, Osborn JW. The effect of normal occlusal forces on fl uid movement through human dentine in vitro. Arch Oral Biol. 2000;45:1033-41.
23. Lee SK, Min KS, Youngho K, Jeong GS, Lee SH, Lee HJ,et al. Mechanical stress activates proinfl ammatory cytokines and antioxidant defense enzymes in human dental pulp cells. J Endod. 2008;34:1364-9.
24. Han MJ, Seo YK, Yoon HH, Song KY, Park JK. Effect of mechanical tension on the human dental pulp cells. Biotechnol Bioproc Eng. 2008;13:410-7.
25. Take I, Kobayashi Y, Yamamoto Y, Tsuboi H, Ochi T, Uematsu S,et al. Prostaglandin E2 strongly inhibits human osteoclast formation 11. Endocrinology. 2005;146:5204-14.
26. Simmons DL, Botting RM, Hla T. Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev. 2004;56:387-437.
27. Zhang X, Schwarz EM, Young DA, Puzas JE, Rosier RN, O Keefe RJ. Cyclooxygenase-2 regulates mesenchymal cell differentiation into the osteoblast lineage and is critically involved in bone repair. J Clin Invest. 2002;109:1405-15.
28. Forwood MR. Inducible cyclo-oxygenase (COX-2) mediates the induction of bone formation by mechanical loading in vivo. J Bone Miner Res. 1996;11:1688-93.
29. Bakker AD, Klein-Nulend J, Burger EH. Mechanotransduction in bone cells proceeds via activation of COX-2, but not COX-1. Biochem Biophys Res Commun. 2003;305:677-83.
30. Joldersma M, Burger EH, Semeins CM, Klein-Nulend J. Mechanical stress induces COX-2 mRNA expression in bone cells from elderly women. J Biomech. 2000;33:53-61.
31. Klein-Nulend J, Helfrich MH, Sterck JG, MacPherson H, Joldersma M, Ralston SH,et al. Nitric oxide response to shear stress by human bone cell cultures is endothelial nitric oxide synthase dependent. Biochem Biophys Res Commun. 1998; 250:108-14.
32. Zaman G, Pitsillides AA, Rawlinson SC, Suswillo RF, Mosley JR, Cheng MZ,et al. Mechanical strain stimulates nitric oxide production by rapid activation of endothelial nitric oxide synthase in osteocytes. J Bone Miner Res. 1999;14:1123-31.
33. Fan X, Roy E, Zhu L, Murphy TC, Ackert-Bicknell C, Hart CM,et al. Nitric oxide regulates receptor activator of nuclear factor-kappaB ligand and osteoprotegerin expression in bone marrow stromal cells. Endocrinology. 2004;145:751-9.
34. Collin-Osdoby P, Rothe L, Bekker S, Anderson F, Osdoby P. Decreased nitric oxide levels stimulate osteoclastogenesis and bone resorption both in vitro and in vivo on the chick chorioallantoic membrane in association with neoangiogenesis. J Bone Miner Res. 2000;15:474-88.
35. Klein-Nulend J, Roelofsen J, Semeins CM, Bronckers ALJJ, Burger EH. Mechanical stimulation of osteopontin mRNA expression and synthesis in bone cell cultures. J Cell Physiol. 1997;170:174-81.
36. You J, Yellowley CE, Donahue HJ, Zhang Y, Chen Q, Jacobs CR. Substrate deformation levels associated with routine physical activity are less stimulatory to bone cells relative to loading-induced oscillatory fl uid fl ow. J Biomech Eng. 2000; 122:387-93.
37. Kim CH, You L, Yellowley CE, Jacobs CR. Oscillatory fl uid fl ow-induced shear stress decreases osteoclastogenesis through RANKL and OPG signaling. Bone. 2006;39:1043-7.
38. Mehrotra M, Saegusa M, Wadhwa S, Voznesensky O, Peterson D, Pilbeam C. Fluid fl ow induces Rankl expression in primary murine calvarial osteoblasts. J Cell Biochem. 2006;98:1271-83.
39. Rubin J, Murphy TC, Zhu L, Roy E, Nanes MS, Fan X. Mechanical strain differentially regulates endothelial nitricoxide synthase and receptor activator of nuclear kappa B ligand expression via ERK1/2 MAPK. J Biol Chem. 2003;278: 34018-25.
40. Knippenberg M, Helder MN, Zandieh-Doulabi B, Semeins CM, Wuisman PIJM, Klein-Nulend J. Adipose tissue-derived mesenchymal stem cells acquire bone cell-like responsiveness to fl uid shear stress on osteogenic stimulation. Tissue Eng. 2005;11:1780-8.
41. Abdallah BM, Haack-Sorensen M, Burns JS, Elsnab B, Jakob F, Hokland P,et al. Maintenance of differentiation potential of human bone marrow mesenchymal stem cells immortalized by human telomerase reverse transcriptase gene despite [corrected] extensive proliferation. Biochem Biophys Res Commun. 2005;326:527-38.
42. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C,et al. A biomarker that identifi es senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA. 1995;92:9363-7.
43. Dominici M, Le BK, Mueller I, Slaper-Cortenbach I, Marini F, Krause D,et al. Minimal criteria for defi ning multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8: 315-7.
44. Bacabac RG, Smit TH, Mullender MG, Dijcks SJ, Van Loon JJWA, Klein-Nulend J. Nitric oxide production by bone cells is fl uid shear stress rate dependent. Biochem Biophys Res Commun. 2004;315:823-9.
45. Abdallah BM, Ditzel N, Kassem M. Assessment of bone formation capacity using in vivo transplantation assays: procedure and tissue analysis. Methods Mol Biol. 2008;455:89-100.
46. Weinbaum S, Cowin SC, Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fl uid shear stresses. J Biomech. 1994;27:339-60.
47. Shi S, Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res. 2003;18:696-704.
48. Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I,et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell. 2007;131:324-36.
49. Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A,et al. Stem cell properties of human dental pulp stem cells. J Dent Res. 2002;81:531-5.
50. Shi S, Robey PG, Gronthos S. Comparison of human dental pulp and bone marrow stromal stem cells by cDNA microarray analysis. Bone. 2001;29:532-9.
51. Carinci F, Papaccio G, Laino G, Palmieri A, Brunelli G, d Aquino R,et al. Comparison between genetic portraits of osteoblasts derived from primary cultures and osteoblasts obtained from human pulpar stem cells. J Craniofacial Surg. 2008;19:616-25.
52. Joldersma M, Klein-Nulend J, Oleksik AM, Heyligers IC, Burger EH. Estrogen enhances mechanical stress-induced prostaglandin production by bone cells from elderly women. Am J Physiol Endocrinol Metab. 2001;280:436-42.
53. Nakanishi T, Shimizu H, Hosokawa Y, Matsuo T. An immunohistological study on cyclooxygenase-2 in human dental pulp. J Endod. 2001;27:385-8.
54. Di Maio FD, Lohinai Z, D A rcangelo C, De Fazio PE, Speranza L, De Lutiis MA,et al. Nitric oxide synthase in healthy and infl amed human dental pulp. J Dent Res. 2004;83:312-6.
55. MacMicking J, Xie QW, Nathan C. Nitric oxide and macrophage function. Ann Rev Immunol. 1997;15:323-50.
56. Uematsu M, Ohara Y, Navas JP, Nishida K, Murphy TJ, Alexander RW,et al. Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress. Am J Physiol Cell Physiol. 1995;38:1371-8.
57. Bakker AD, Klein-Nulend J, Tanck E, Albers GH, Lips P, Burger EH. Additive effects of estrogen and mechanical stress on nitric oxide and prostaglandin E2 production by bone cells from osteoporotic donors. Osteoporos Int. 2005; 16:983-9.
58. Tjabringa GS, Vezeridis PS, Zandieh-Doulabi B, Helder MN, Wuisman PIJM, Klein-Nulend J. Polyamines modulate nitric oxide production and COX-2 gene expression in response to mechanical loading in human adipose tissue-derived mesenchymal stem cells. Stem Cells. 2006;24:2262-9.
59. Allard B, Couble ML, Magloire H, Bleicher F. Characterization and gene expression of high conductance calciumactivated potassium channels displaying mechanosensitivity in human odontoblasts. J Biol Chem. 2000;275:25556-61
60. Charoenlarp P, Wanachantararak S, Vongsavan N, Matthews B. Pain and the rate of dentinal fl uid fl ow produced by hydrostatic pressure stimulation of exposed dentine in man. Arch Oral Biol. 2007;625-31.
61. Mei YF, Yamaza T, Atsuta I, Danjo A, Yamashita Y, Kido MA,et al. Sequential expression of endothelial nitric oxide synthase, inducible nitric oxide synthase, and nitrotyrosine in odontoblasts and pulp cells during dentin repair after tooth preparation in rat molars. Cell Tissue Res. 2007; 328:117-27.
62. Hirao M, Hashimoto J, Yamasaki N, Ando W, Tsuboi H, Myoui A,et al. Oxygen tension is an important mediator of the transformation of osteoblasts to osteocytes. J Bone Miner Metab. 2007;25:266-76.
63. Ponik SM, Triplett JW, Pavalko FM. Osteoblasts and osteocytes respond differently to oscillatory and unidirectional fl uid fl ow profi les. J Cell Biochem. 2007;100:794-807.
64. Rahnert J, Fan X, Case N, Murphy TC, Grassi F, Sen B,et al. The role of nitric oxide in the mechanical repression of RANKL in bone stromal cells. Bone. 2008;43:48-53.