Cell death, cavitation and spontaneous multi-differentiation of dental pulp stem cells-derived spheroids in vitro: A journey to survival and organogenesis

Biology of the Cell

Volumn 106, Issue 12, 2014, Pages 405-419

  Xiao, Li ^a   Kumazawa, Yasuo ^a   Okamura, Hisashi ^a  

^a NIPPON DENTAL UNIVERSITY   (Japan)

Author keywords

Cartilage; Cavitation; Neurogenesis; Osteogenesis; Spheroid

Indexed keywords

ALKALINE PHOSPHATASE; CELL MARKER; FIBROBLAST GROWTH FACTOR 3; OSTEOGENIC PROTEIN 1; STRO 1 PROTEIN; UNCLASSIFIED DRUG; COLLAGEN; CULTURE MEDIUM; DIFFERENTIATION ANTIGEN; DRUG COMBINATION; KI 67 ANTIGEN; LAMININ; MATRIGEL; PROTEOGLYCAN;

ARTICLE; BIOLOGICAL FUNCTIONS; CELL CAVITATION; CELL DEATH; CELL DIFFERENTIATION; CELL FUNCTION; CELL HYPOXIA; CELL LINEAGE; CELL SURVIVAL; CONTROLLED STUDY; DENTAL PULP STEM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; ORGANOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPHEROID CELL; TISSUE REGENERATION; ADOLESCENT; ADULT; ADULT STEM CELL; ANGIOGENESIS; BONE MINERALIZATION; CULTURE MEDIUM; CULTURE TECHNIQUE; CYTOLOGY; DRUG COMBINATION; EMBRYOLOGY; GENE EXPRESSION PROFILING; METABOLISM; MOLAR TOOTH; MULTICELLULAR SPHEROID; PHARMACOLOGY; PHYSIOLOGY; PLURIPOTENT STEM CELL; TOOTH PULP; YOUNG ADULT;

ADOLESCENT; ADULT; ADULT STEM CELLS; ANTIGENS, DIFFERENTIATION; CALCIFICATION, PHYSIOLOGIC; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL HYPOXIA; CELL LINEAGE; CELL SURVIVAL; COLLAGEN; CULTURE MEDIA; DENTAL PULP; DRUG COMBINATIONS; GENE EXPRESSION PROFILING; HUMANS; KI-67 ANTIGEN; LAMININ; MOLAR, THIRD; NEOVASCULARIZATION, PHYSIOLOGIC; ORGANOGENESIS; PLURIPOTENT STEM CELLS; PROTEOGLYCANS; SPHEROIDS, CELLULAR; YOUNG ADULT;

EID: 84918780117     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1111/boc.201400024     Document Type: Article

References (52)

1. Abcam. Whole mount fluorescent immunohistochemistry. Available at http://www.abcam.com/ps/pdf/protocols/whole_mount_fluorescent_ihc.pdf. Assessed 24 March 2014
2. Alexander, R.E., Cheng, L., Grignon, D.J. and Idrees, M.T. (2014) Cytoplasmic OCT4 staining is a sensitive marker of neuroendocrine differentiation. Hum. Pathol. 45, 27-32
3. Ameisen, J.C. (2002). On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ. 9, 367-393
4. Angelo, G. and Van Gilst, M.R. (2009). Starvation protects germline stem cells and extends reproductive longevity in C. elegans. Science 326, 954-958
5. Bates, R.C., Edwards, N.S. and Yates, J.D. (2000). Spheroids and cell survival. Crit. Rev. Oncol. Hematol. 36, 61-74
6. Bialas, M., Krupka, M., Janeczek, A., Rozwadowska, N., Fraczek, M., Kotlinowski, J., Kucharzewska, P., Lackowska, B. and Kurpisz, M. (2011). Transient and stable transfections of mouse myoblasts with genes coding for pro-angiogenic factors. J. Physiol. Pharmacol. 62, 219-228
7. Calvi, L.M., Adams, G.B., Weibrecht, K.W., Weber, J.M., Olson, D.P., Knight, M.C., Martin, R.P., Schipani, E., Divieti, P., Bringhurst, F.R., Milner, L.A., Kronenberg, H.M. and Scadden, D.T. (2003). Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841-846.
8. Coucouvanis, E. and Martin, G.R. (1995). Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 83, 279-287
9. Coucouvanis, E. and Martin, G.R. (1999). BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development 126, 535-546
10. Dainiak, N. (1991). Surface membrane-associated regulation of cell assembly, differentiation, and growth. Blood 78, 264-276
11. d'Aquino, R., Graziano, A., Sampaolesi, M., Laino, G., Pirozzi, G., De Rosa, A. and 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
12. Desoize, B., Gimonet, D. and Jardiller, J.C. (1998). Cell culture as spheroids: an approach to multicellular resistance. Anticancer Res. 18, 4147-4158
13. Esner, M., Pachernik, J., Hampl, A. and Dvorak, P. (2002). Targeted disruption of fibroblast growth factor receptor-1 blocks maturation of visceral endoderm and cavitation in mouse embryoid bodies. Int. J. Dev. Biol. 46, 817-825
14. Friedrich, J., Ebner, R. and Kunz-Schughart, L.A. (2007). Experimental anti-tumor therapy in 3-D: spheroids-old hat or new challenge? Int. J. Radiat. Biol. 83, 849-871
15. Golpour, M., Fattahi, S., Niaki, H.A., Hadipoor, A., Abedian, Z., Ahangarian, G.R., Parsian, H., Mosapour, A., Khorasani, H.R., Vaziri, H.R., Bijani, A. and Mostafazadeh, A. (2014). Starved human fibroblasts secrete acidic proteins inducing post re-feeding proliferation and in vitro cell migration: a potential tool for wound healing. Biol. Cell 106, 139-150
16. Gronthos, S., Mankani, M., Brahim, J., Robey, P.G. and Shi, S. (2000). Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 97, 13625-13630
17. Guerrero, I. and Altaba, A.R. (2003). Longing for ligand: hedgehog, patched, and cell death. Science 301, 774-776
18. Heneidi, S., Simerman, A.A., Keller, E., Singh, P., Li, X., Dumesic, D.A. and Chazenbalk, G. (2013). Awakened by cellular stress: isolation and characterization of a novel population of pluripotent stem cells derived from human adipose tissue. PLoS One 8, e64752
19. Hernández-García, D., Castro-Obregón, S., Gómez-López, S., Valencia, C. and Covarrubias, L. (2008). Cell death activation during cavitation of embryoid bodies is mediated by hydrogen peroxide. Exp. Cell Res. 314, 2090-2099
20. Hipfner, D.R. and Cohen, S.M. (2004). Connecting proliferation and apoptosis in development and disease. Nat. Rev. Mol. Cell Biol. 5, 805-815
21. Hirschhaeuser, F., Menne, H., Dittfeld, C., West, J., Mueller-Klieser, W. and Kunz-Schughart, L.A. (2010). Multicellular tumor spheroids: an underestimated tool is catching up again. J. Biotechnol. 148, 3-15
22. Huang, G.T., Gronthos, S. and Shi, S. (2009). Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J. Dent. Res. 88, 792-806
23. Ishkitiev, N., Yaegaki, K., Kozhuharova, A., Tanaka, T., Okada, M., Mitev, V., Fukuda, M. and Imai, T. (2013). Pancreatic differentiation of human dental pulp CD117 stem cells. Regen. Med. 8, 597-612
24. Kanczler, J.M. and Oreffo, R.O. (2008). Osteogenesis and angiogenesis: the potential for engineering bone. Eur. Cell Mater. 15, 100-114
25. Kuroda, Y., Kitada, M., Wakao, S., Nishikawa, K., Tanimura, Y., Makinoshima, H., Goda, M., Akashi, H., Inutsuka, A., Niwa, A., Shigemoto, T., Nabeshima, Y., Nakahata, T., Nabeshima, Y., Fujiyoshi, Y. and Dezawa, M. (2010). Unique multipotent cells in adult human mesenchymal cell populations. Proc. Natl. Acad. Sci. U.S.A. 107, 8639-8643
26. Lin, G., Liu, G., Banie, L., Wang, G., Ning, H., Lue, T.F. and Lin, C.S. (2011). Tissue distribution of mesenchymal stem cell marker Stro-1. Stem Cells Dev. 20, 1747-1752
27. Mannello, F., Medda, V. and Tonti, G.A. (2011). Hypoxia and neural stem cells: from invertebrates to brain cancer stem cells. Int. J. Dev. Biol. 55, 569-581
28. Mascré, G., Dekoninck, S., Drogat, B., Youssef, K.K., Broheé, S., Sotiropoulou, P.A., Simons, B.D. and Blanpain, C. (2012). Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 489, 257-262
29. Nechiporuk, A., Linbo, T. and Raible, D.W. (2005). Endoderm-derived Fgf3 is necessary and sufficient for inducing neurogenesis in the epibranchial placodes in zebrafish. Development 132, 3717-3730
30. Ning, H., Lin, G., Lue, T.F. and Lin, C.S. (2011). Mesenchymal stem cell marker Stro-1 is a 75 kd endothelial antigen. Biochem. Biophys. Res. Commun. 413, 353-357
31. O'Connor, M.D., Kardel, M.D., Iosfina, I., Youssef, D., Lu, M., Li, M.M., Vercauteren, S., Nagy, A. and Eaves, C.J. (2008). Alkaline phosphatase-positive colony formation is a sensitive, specific, and quantitative indicator of undifferentiated human embryonic stem cells. Stem Cells 26, 1109-1116.
32. O'Reilly, L.P., Watkins, S.C. and Smithgall, T.E. (2011) An unexpected role for the clock protein timeless in developmental apoptosis. PLoS One 6, e17157
33. Raff, M.C., Barres, B.A., Burne, J.F., Coles, H.S., Ishizaki, Y. and Jacobson, M.D. (1993). Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262, 695-700
34. Santini, M.T. and Rainaldi, G. (1999). Three-dimensional spheroid model in tumor biology. Pathobiology 67, 148-157
35. Saunders, J.W. (1966). Death in embryonic systems. Science 154, 604-612
36. Shepard, T.H., Muffley, L.A. and Smith, L.T. (1998). Ultrastructural study of mitochondria and their cristae in embryonic rats and primate (N. nemistrina). Anat. Rec. 252, 383-392
37. Simon, M.C. and Keith, B. (2008). The role of oxygen availability in embryonic development and stem cell function. Nat. Rev. Mol. Cell Biol. 9, 285-296
38. Sodunke, T.R., Turner, K.K., Caldwell, S.A., McBride, K.W., Reginato, M.J. and Noh, H.M. (2007). Micropatterns of Matrigel for three-dimensional epithelial cultures. Biomaterials 28, 4006-4016
39. Spence, J.R., Mayhew, C.N., Rankin, S.A., Kuhar, M.F., Vallance, J.E., Tolle, K., Hoskins, E.E., Kalinichenko, V.V., Wells, S.I., Zorn, A.M., Shroyer, N.F. and Wells, J.M. (2011). Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 470, 105-109
40. Stange, D.E., Koo, B.K., Huch, M., Sibbel, G., Basak, O., Lyubimova, A., Kujala, P., Bartfeld, S., Koster, J., Geahlen, J.H., Peters, P.J., van Es, J.H., van de Wetering, M., Mills, J.C. and Clevers, H. (2013). Differentiated Troy+ chief cells act as reserve stem cells to generate all lineages of the stomach epithelium. Cell 155, 357-368
41. Suda, T., Takubo, K. and Semenza, G.L. (2011). Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell 9, 298-310
42. Takenobu, H., Shimozato, O., Nakamura, T., Ochiai, H., Yamaguchi, Y., Ohira, M., Nakagawara, A. and Kamijo, T. (2011). CD133 suppresses neuroblastoma cell differentiation via signal pathway modification. Oncogene 30, 97-105
43. Tata, P.R., Mou, H., Pardo-Saganta, A., Zhao, R., Prabhu, M., Law, B.M., Vinarsky, V., Cho, J.L., Breton, S., Sahay, A., Medoff, B.D. and Rajagopal, J. (2013). Dedifferentiation of committed epithelial cells into stem cells in vivo. Nature 503, 218-223
44. Tra, T., Gong, L., Kao, L.P., Li, X.L., Grandela, C., Devenish, R.J., Wolvetang, E. and Prescott, M. (2011). Autophagy in human embryonic stem cells. PLoS One 6, e27485
45. Tsutsui, T.W., Inaba, T., Fisher, L.W., Robey, P.G. and Tsutsui, T. (2006). In vitro chromosome aberration tests using human dental pulp cells to detect the carcinogenic potential of chemical agents. Odontology 94, 44-50
46. Webster, D.M., Teo, C.F., Sun, Y., Wloga, D., Gay, S., Klonowski, K.D., Wells, L. and Dougan, S.T. (2009). O-GlcNAc modifications regulate cell survival and epiboly during zebrafish development. BMC Dev. Biol. 9, 28
47. Wu, X., Ferrara, C., Shapiro, E. and Grishina, I. (2009). Bmp7 expression and null phenotype in the urogenital system suggest a role in re-organization of the urethral epithelium. Gene Expr. Patterns 9, 224-230
48. Xiao, L. and Tsutsui, T. (2012). Three-dimensional epithelial and mesenchymal cell co-cultures form early tooth epithelium invagination-like structures: expression patterns of relevant molecules. J. Cell. Biochem. 113, 1875-1885
49. Xu, K., Wu, X., Shapiro, E., Huang, H., Zhang, L., Hickling, D., Deng, Y., Lee, P., Li, J., Lepor, H. and Grishina, I. (2012). Bmp7 functions via a polarity mechanism to promote cloacal septation. PLoS One 7, e29372
50. Yamagata, K., Ueda, J., Mizutani, E., Saitou, M. and Wakayama, T. (2010). Survival and death of epiblast cells during embryonic stem cell derivation revealed by long-term live-cell imaging with an Oct4 reporter system. Dev. Biol. 346, 90-101
51. Zhou, Y., Li, S., Huang, Q., Xie, L. and Zhu, X. (2013). Nanog suppresses cell migration by downregulating thymosin β4 and Rnd3. J. Mol. Cell. Biol. 5, 239-249
52. Zylbersztejn, K. and Galli, T. (2011). Vesicular traffic in cell navigation. FEBS J. 278, 4497-4505