Characterization of canine dental pulp cells and their neuroregenerative potential

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• 作者：Eiji Naito ; Daichi Kudo ; Shin-ichiro Sekine…
• 关键词：Dental pulp cells ; Mesenchymal stem cells ; Neurotrophic factors ; Neurite outgrowth ; Superparamagnetic iron oxide
• 刊名：In Vitro Cellular & Developmental Biology - Animal
• 出版年：2015
• 出版时间：November 2015
• 年：2015
• 卷：51
• 期：10
• 页码：1012-1022
• 全文大小：1,264 KB
• 参考文献：Alge DL, Zhou D, Adams LL, Wyss BK, Shadday MD, Woods EJ, Gabriel Chu TM, Goebel WS (2010) Donor-matched comparison of dental pulp stem cells and bone marrow-derived mesenchymal stem cells in a rat model. J Tissue Eng Regen Med 4:73鈥?1PubMedCentral PubMed
  Arbab AS, Bashaw LA, Miller BR, Jordan EK, Lewis BK, Kalish H, Frank JA (2003) Characterization of biophysical and metabolic properties of cells labeled with superparamagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. Radiology 229:838鈥?46CrossRef PubMed
  Arthur A, Rychkov G, Shi S, Koblar SA, Gronthos S (2008) Adult human dental pulp stem cells differentiate toward functionally active neurons under appropriate environmental cues. Stem Cells 26:1787鈥?795CrossRef PubMed
  Azizi SA, Stokes D, Augelli BJ, DiGirolamo C, Prockop DJ (1998) Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats鈥攕imilarities to astrocyte grafts. Proc Natl Acad Sci U S A 95:3908鈥?913PubMedCentral CrossRef PubMed
  Banas A, Teratani T, Yamamoto Y, Tokuhara M, Takeshita F, Quinn G, Okochi H, Ochiya T (2007) Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. Hepatology 46:219鈥?28CrossRef PubMed
  Belliveau DJ, Krivko I, Kohn J, Lachance C, Pozniak C, Rusakov D, Kaplan D, Miller FD (1997) NGF and neurotrophin-3 both activate TrkA on sympathetic neurons but differentially regulate survival and neuritogenesis. J Cell Biol 136:375鈥?88PubMedCentral CrossRef PubMed
  Bratka-Robia CB, Mitteregger G, Aichinger A, Egerbacher M, Helmreich M, Bamberg E (2002) Primary cell culture and morphological characterization of canine dermal papilla cells and dermal fibroblasts. Vet Dermatol 13:1鈥?CrossRef PubMed
  Bull E, Madani SY, Sheth R, Seifalian A, Green M, Seifalian AM (2014) Stem cell tracking using iron oxide nanoparticles. Int J Nanomedicine 9:1641鈥?653PubMedCentral PubMed
  Chamberlain G, Fox J, Ashton B, Middleton J (2007) Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25:2739鈥?749CrossRef PubMed
  Chao MV (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4:299鈥?09CrossRef PubMed
  Clary DO, Reichardt LF (1994) An alternatively spliced form of the nerve growth factor receptor TrkA confers an enhanced response toneurotrophin 3. Proc Natl Acad Sci U S A 91:11133鈥?1137PubMedCentral CrossRef PubMed
  de Almeida FM, Marques SA, Ramalho BS, Rodrigues RF, Cadilhe DV, Furtado D, Kerkis I, Pereira LV, Rehen SK, Martinez AM (2011) Human dental pulp cells: a new source of cell therapy in a mouse model of compressive spinal cord injury. J Neurotrauma 28:1939鈥?949CrossRef PubMed
  Dissanayaka WL, Zhu X, Zhang C, Jin L (2011) Characterization of dental pulp stem cells isolated from canine premolars. J Endod 37:1074鈥?080CrossRef PubMed
  Ellis KM, O鈥機arroll DC, Lewis MD, Rychkov GY, Koblar SA (2014) Neurogenic potential of dental pulp stem cells isolated from murine incisors. Stem Cell Res Ther 5:30PubMedCentral CrossRef PubMed
  Encinas M, Iglesias M, Llecha N, Comella JX (1999) Extracellular-regulated kinases and phosphatidylinositol 3-kinase are involved in brain-derived neurotrophic factor-mediated survival and neuritogenesis of the neuroblastoma cell line SH-SY5Y. J Neurochem 73:1409鈥?421CrossRef PubMed
  Gronthos S, Mankani M, Brahim J, Robey PG, Shi S (2000) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci U S A 97:13625鈥?3630PubMedCentral CrossRef PubMed
  Himmelreich U, Dresselaers T (2009) Cell labeling and tracking for experimental models using magnetic resonance imaging. Methods 48:112鈥?24CrossRef PubMed
  Hu SL, Zhang JQ, Hu X, Hu R, Luo HS, Li F, Xia YZ, Li JT, Lin JK, Zhu G, Feng H (2009) In vitro labeling of human umbilical cord mesenchymal stem cells with superparamagnetic iron oxide nanoparticles. J Cell Biochem 108:529鈥?35CrossRef PubMed
  Ip NY, Stitt TN, Tapley P, Klein R, Glass DJ, Fandl J, Greene LA, Barbacid M, Yancopoulos GD (1993) Similarities and differences in the way neurotrophins interact with the Trk receptors in neuronal and nonneuronal cells. Neuron 10:137鈥?49CrossRef PubMed
  Jaiswal N, Haynesworth SE, Caplan AI, Bruder SP (1997) Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 64:295鈥?12CrossRef PubMed
  Jendelov谩 P, Herynek V, Urdz铆kov谩 L, Glogarov谩 K, Kroupov谩 J, Andersson B, Bryja V, Burian M, H谩jek M, Sykov谩 E (2004) Magnetic resonance tracking of transplanted bone marrow and embryonic stem cells labeled by iron oxide nanoparticles in rat brain and spinal cord. J Neurosci Res 76:232鈥?43CrossRef PubMed
  Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41鈥?9CrossRef PubMed
  Jones BJ, McTaggar SJ (2008) Immunosuppression by mesenchymal stromal cells: from culture to clinic. Exp Hematol 36:733鈥?41CrossRef PubMed
  Kamishina H, Deng J, Oji T, Cheeseman JA, Clemmons RM (2006) Expression of neural markers on bone marrow-derived canine mesenchymal stem cells. Am J Vet Res 67:1921鈥?928CrossRef PubMed
  Karussis D, Kassis I, Kurkalli BG, Slavin S (2008) Immunomodulation and neuroprotection with mesenchymal bone marrow stem cells (MSCs): a proposed treatment for multiple sclerosis and other neuroimmunological/neurodegenerative diseases. J Neurol Sci 265:131鈥?35CrossRef PubMed
  Kern S, Eichler H, Stoeve J, Kl眉ter H, Bieback K (2006) Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24:1294鈥?301CrossRef PubMed
  Kir谩ly M, Porcsalmy B, Pataki A, K谩d谩r K, Jelitai M, Moln谩r B, Hermann P, Gera I, Grimm WD, Ganss B, Zsembery A, Varga G (2009) Simultaneous PKC and cAMP activation induces differentiation of human dental pulp stem cells into functionally active neurons. Neurochem Int 55:323鈥?32CrossRef PubMed
  Kir谩ly M, K谩d谩r K, Horv谩thy DB, Nardai P, R谩cz GZ, Lacza Z, Varga G, Gerber G (2011) Integration of neuronally predifferentiated human dental pulp stem cells into rat brain in vivo. Neurochem Int 59:371鈥?81CrossRef PubMed
  Komada Y, Yamane T, Kadota D, Isono K, Takakura N, Hayashi S, Yamazaki H (2012) Origins and properties of dental, thymic, and bone marrow mesenchymal cells and their stem cells. PLoS One 7, e46436PubMedCentral CrossRef PubMed
  Kuruvilla R, Zweifel LS, Glebova NO, Lonze BE, Valdez G, Ye H, Ginty DD (2004) A neurotrophin signaling cascade coordinates sympathetic neuron development through differential control of TrkA trafficking and retrograde signaling. Cell 118:243鈥?55CrossRef PubMed
  Levy YS, Gilgun-Sherki Y, Melamed E, Offen D (2005) Therapeutic potential of neurotrophic factors in neurodegenerative diseases. BioDrugs 19:97鈥?27CrossRef PubMed
  Lillesaar C, Eriksson C, Fried K (2001) Rat tooth pulp cells elicit neurite growth from trigeminal neurones and express mRNAs for neurotrophic factors in vitro. Neurosci Lett 308:161鈥?64CrossRef PubMed
  Lunov O, Syrovets T, B眉chele B, Jiang X, R枚cker C, Tron K, Nienhaus GU, Walther P, Mail盲nder V, Landfester K, Simmet T (2010) The effect of carboxydextran-coated superparamagnetic iron oxide nanoparticles on c-Jun N-terminal kinase-mediated apoptosis in human macrophages. Biomaterials 31:5063鈥?071CrossRef PubMed
  Martens W, Bronckaers A, Politis C, Jacobs R, Lambrichts I (2013) Dental stem cells and their promising role in neural regeneration: an update. Clin Oral Investig 17:1969鈥?983CrossRef PubMed
  Mead B, Logan A, Berry M, Leadbeater W, Scheven BA (2013) Intravitreally transplanted dental pulp stem cells promote neuroprotection and axon regeneration of retinal ganglion cells after optic nerve injury. Invest Ophthalmol Vis Sci 54:7544鈥?556CrossRef PubMed
  Mead B, Logan A, Berry M, Leadbeater W, Scheven BA (2014) Paracrine-mediated neuroprotection and neuritogenesis of axotomised retinal ganglion cells by human dental pulp stem cells: comparison with human bone marrow and adipose-derived mesenchymal stem cells. PLoS One 9, e109305PubMedCentral CrossRef PubMed
  Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S (2003) SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A 100:5807鈥?812PubMedCentral CrossRef PubMed
  Mohiuddin L, Fernandez K, Tomlinson DR, Fernyhough P (1995) Nerve growth factor and neurotrophin-3 enhance neurite outgrowth and up-regulate the levels of messenger RNA for growth-associated protein GAP-43 and T alpha 1 alpha-tubulin in cultured adult rat sensory neurones. Neurosci Lett 185:20鈥?3CrossRef PubMed
  Morfini G, DiTella MC, Feiguin F, Carri N, C谩ceres A (1994) Neurotrophin-3 enhances neurite outgrowth in cultured hippocampal pyramidal neurons. J Neurosci Res 39:219鈥?32CrossRef PubMed
  Nosrat CA, Fried K, Lindskog S, Olson L (1997) Cellular expression of neurotrophin mRNAs during tooth development. Cell Tissue Res 290:569鈥?80CrossRef PubMed
  Nosrat IV, Widenfalk J, Olson L, Nosrat CA (2001) Dental pulp cells produce neurotrophic factors, interact with trigeminal neurons in vitro, and rescue motoneurons after spinal cord injury. Dev Biol 238:120鈥?32CrossRef PubMed
  Nosrat IV, Smith CA, Mullally P, Olson L, Nosrat CA (2004) Dental pulp cells provide neurotrophic support for dopaminergic neurons and differentiate into neurons in vitro; implications for tissue engineering and repair in the nervous system. Eur J Neurosci 19:2388鈥?398CrossRef PubMed
  Omidkhoda A, Mozdarani H, Movasaghpoor A, Fatholah AA (2007) Study of apoptosis in labeled mesenchymal stem cells with superparamagnetic iron oxide using neutral comet assay. Toxicol In Vitro 21:1191鈥?196CrossRef PubMed
  Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143鈥?47CrossRef PubMed
  Reyes M, Verfaillie CM (2001) Characterization of multipotent adult progenitor cells, a subpopulation of mesenchymal stem cells. Ann N Y Acad Sci 938:231鈥?33
  Sakai K, Yamamoto A, Matsubara K, Nakamura S, Naruse M, Yamagata M, Sakamoto K, Tauchi R, Wakao N, Imagama S, Hibi H, Kadomatsu K, Ishiguro N, Ueda M (2012) Human dental pulp-derived stem cells promote locomotor recovery after complete transection of the rat spinal cord by multiple neuro-regenerative mechanisms. J Clin Invest 122:80鈥?0PubMedCentral PubMed
  Sch盲fer R, Bantleon R, Kehlbach R, Siegel G, Wiskirchen J, Wolburg H, Kluba T, Eibofner F, Northoff H, Claussen CD, Schlemmer HP (2010) Functional investigations on human mesenchymal stem cells exposed to magnetic fields and labeled with clinically approved iron nanoparticles. BMC Cell Biol 11:22PubMedCentral CrossRef PubMed
  Schmidt CE, Shastri VR, Vacanti JP, Langer R (1997) Stimulation of neurite outgrowth using an electrically conducting polymer. Proc Natl Acad Sci U S A 94:8948鈥?953PubMedCentral CrossRef PubMed
  Strohmaier C, Carter BD, Urfer R, Barde YA, Dechant G (1996) A splice variant of the neurotrophin receptor trkB with increased specificity for brain-derived neurotrophic factor. EMBO J 15:3332鈥?337PubMedCentral PubMed
  Struys T, Ketkar-Atre A, Gervois P, Leten C, Hilkens P, Martens W, Bronckaers A, Dresselaers T, Politis C, Lambricht I, Himmelreich U (2013) Magnetic resonance imaging of human dental pulp stem cells in vitro and in vivo. Cell Transplant 22:1813鈥?829CrossRef PubMed
  Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD (2002) Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105:93鈥?8CrossRef PubMed
  Tsoulfas P, Soppet D, Escandon E, Tessarollo L, Mendoza-Ramirez JL, Rosenthal A, Nikolics K, Parada LF (1993) The rat trkC locus encodes multiple neurogenic receptors that exhibit differential response to neurotrophin-3 in PC12 cells. Neuron 10:975鈥?90CrossRef PubMed
  Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W, Ho AD (2005) Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 33:1402鈥?416CrossRef PubMed
  Wang X, Wei F, Liu A, Wang L, Wang JC, Ren L, Liu W, Tu Q, Li L, Wang J (2012) Cancer stem cell labeling using poly(L-lysine)-modified iron oxide nanoparticles. Biomaterials 33:3719鈥?732CrossRef PubMed
  Yang JX, Tang WL, Wang XX (2010) Superparamagnetic iron oxide nanoparticles may affect endothelial progenitor cell migration ability and adhesion capacity. Cytotherapy 12:251鈥?59CrossRef PubMed
  Zhu MT, Wang Y, Feng WY, Wang B, Wang M, Ouyang H, Chai ZF (2010) Oxidative stress and apoptosis induced by iron oxide nanoparticles in cultured human umbilical endothelial cells. J Nanosci Nanotechnol 10:8584鈥?590CrossRef PubMed
  
• 作者单位：Eiji Naito (1)
  Daichi Kudo (2)
  Shin-ichiro Sekine (2)
  Kazuhiro Watanabe (1)
  Yui Kobatake (1)
  Naritaka Tamaoki (3)
  Masatoshi Inden (2)
  Kazuki Iida (3)
  Yusuke Ito (1)
  Isao Hozumi (2)
  Toshiyuki Shibata (3)
  Sadatoshi Maeda (1)
  Hiroaki Kamishina (1)
  
  1. Department of Veterinary Medicine, Faculty Applied Biological Sciences, Gifu University, 1-1 Yanagido, Gifu, 501-1193, Japan
  2. Laboratory of Medical Therapeutics and Molecular Therapeutics, Gifu Pharmaceutical University, Gifu, Japan
  3. Department of Oral and Maxillofacial Surgery, Graduate School of Medicine, Gifu University, 1-1 Yanagido, Gifu, 501-1193, Japan
  
• 刊物主题：Cell Biology; Developmental Biology; Stem Cells; Cell Culture; Animal Genetics and Genomics;
• 出版者：Springer US
• ISSN：1543-706X

文摘

Dental pulp cells (DPCs) of various species have been studied for their potentials of differentiation into functional neurons and secretion of neurotrophic factors. In canine, DPCs have only been studied for cell surface markers and differentiation, but there is little direct evidence for therapeutic potentials for neurological disorders. The present study aimed to further characterize canine DPCs (cDPCs), particularly focusing on their neuroregenerative potentials. It was also reported that superparamagnetic iron oxide (SPIO) particles were useful for labeling of MSCs and tracking with magnetic resonance imaging (MRI). Our data suggested that cDPCs hold higher proliferation capacity than bone marrow stromal cells, the other type of mesenchymal stem cells which have been the target of intensive research. Canine DPCs constitutively expressed neural markers, suggesting a close relationship to the nervous system in their developmental origin. Canine DPCs promoted neuritogenesis of PC12 cells, most likely through secretion of neurotrophic factors. Furthermore, SPIO nanoparticles could be effectively transported to cDPCs without significant cytotoxicity and unfavorable effects on neuritogenesis. SPIO-labeled cDPCs embedded in agarose spinal cord phantoms were successfully visualized with a magnetic resonance imaging arousing a hope for noninvasive cell tracking in transplantation studies. Keywords Dental pulp cells Mesenchymal stem cells Neurotrophic factors Neurite outgrowth Superparamagnetic iron oxide