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Phenotypic characterization of craniofacial bone marrow stromal cells: unique properties of enhanced osteogenesis, cell recruitment, autophagy, and apoptosis resistance

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Abstract

Previous studies have shown that craniofacial bone marrow stromal cells (MSCs) have greater osteogenic potential than appendicular bone MSCs. However, detailed phenotypic characterization of MSCs from bone marrow in the different sites remains unclear. To investigate bone repair and regeneration of craniofacial MSCs and the regulatory mechanisms underlying their unique properties, we compared osteogenesis, cell recruitment, autophagy, and apoptosis resistance of MSCs from the mandible (M-MSCs) to those from tibia (T-MSCs) in vitro and in vivo. Compared with T-MSCs, M-MSCs formed more colonies, possessed stronger proliferation activity, exhibited higher expression of pluripotency genes such as Oct4 and Nanog, and held stronger osteogenic differentiation in osteogenic medium. Moreover, M-MSCs had greater autophagy and anti-apoptotic capacities than T-MSCs under hypoxia and serum deprivation conditions. M-MSCs were found to be more capable of recruiting more MSCs than T-MSCs. When these MSCs were transplanted into mandible critical-sized defects, more bone formed in the M-MSC-treated animals than in their T-MSC counterparts. Collectively, these findings reveal that MSCs have unique characteristics and bone-repairing properties from the mandible as compared with those from tibia, presumably by enhanced osteogenic potential, cell recruitment, autophagy and apoptosis resistance.

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References

  • Aghaloo TL, Chaichanasakul T, Bezouglaia O, Kang B, Franco R, Dry SM, Atti E, Tetradis S (2010) Osteogenic potential of mandibular vs. long-bone marrow stromal cells. J Dent Res 89(11):1293–1298

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Akintoye SO, Lam T, Shi S, Brahim J, Collins MT, Robey PG (2006) Skeletal site-specific characterization of orofacial and iliac crest human bone marrow stromal cells in same individuals. Bone 38(6):758–768

    Article  PubMed  CAS  Google Scholar 

  • Chai Y, Jiang X, Ito Y, Bringas PJ, Han J, Rowitch DH, Soriano P, McMahon AP, Sucov HM (2000) Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127(8):1671–1679

    PubMed  CAS  Google Scholar 

  • 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(11):2739–2749

    Article  PubMed  CAS  Google Scholar 

  • Chang H, Docheva D, Knothe UR, Knothe TM (2014) Arthritic periosteal tissue from joint replacement surgery: a novel, autologous source of stem cells. Stem Cells Transl Med 3(3):308–317

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cordero DR, Brugmann S, Chu Y, Bajpai R, Jame M, Helms JA (2011) Cranial neural crest cells on the move: their roles in craniofacial development. Am J Med Genet A 155A(2):270–279

    Article  PubMed  Google Scholar 

  • D’Aquino R, Tirino V, Desiderio V, Studer M, De Angelis GC, Laino L, De Rosa A, Di Nucci D, Martino S, Paino F, Sampaolesi M, Papaccio G (2011) Human neural crest-derived postnatal cells exhibit remarkable embryonic attributes either in vitro or in vivo. Eur Cell Mater 21:304–316

    PubMed  Google Scholar 

  • Garcia-de-Alba C, Becerril C, Ruiz V, Gonzalez Y, Reyes S, Garcia-Alvarez J, Selman M, Pardo A (2010) Expression of matrix metalloproteases by fibrocytes: possible role in migration and homing. Am J Respir Crit Care Med 182(9):1144–1152

    Article  PubMed  CAS  Google Scholar 

  • Gibbons J, Hewitt E, Gardner DK (2006) Effects of oxygen tension on the establishment and lactate dehydrogenase activity of murine embryonic stem cells. Cloning Stem Cells 8(2):117–122

    Article  PubMed  CAS  Google Scholar 

  • Gronthos S, Zannettino AC, Hay SJ, Shi S, Graves SE, Kortesidis A, Simmons PJ (2003) Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 116(Pt 9):1827–1835

    Article  PubMed  CAS  Google Scholar 

  • Hearn CJ, Young HM, Ciampoli D, Lomax AE, Newgreen D (1999) Catenary cultures of embryonic gastrointestinal tract support organ morphogenesis, motility, neural crest cell migration, and cell differentiation. Dev Dyn 214(3):239–247

    Article  PubMed  CAS  Google Scholar 

  • Helms JA, Schneider RA (2003) Cranial skeletal biology. Nature 423(6937):326–331

    Article  PubMed  CAS  Google Scholar 

  • Izadpanah R, Trygg C, Patel B, Kriedt C, Dufour J, Gimble JM, Bunnell BA (2006) Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem 99(5):1285–1297

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Javazon EH, Colter DC, Schwarz EJ, Prockop DJ (2001) Rat marrow stromal cells are more sensitive to plating density and expand more rapidly from single-cell-derived colonies than human marrow stromal cells. Stem Cells 19:219–225

  • Jiang X, Zhao J, Wang S, Sun X, Zhang X, Chen J, Kaplan DL, Zhang Z (2009) Mandibular repair in rats with premineralized silk scaffolds and BMP-2-modified bMSCs. Biomaterials 30(27):4522–4532

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kern S, Eichler H, Stoeve J, Kluter H, Bieback K (2006) Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24(5):1294–1301

    Article  PubMed  CAS  Google Scholar 

  • Koole R (1994) Ectomesenchymal mandibular symphysis bone graft: an improvement in alveolar cleft grafting? Cleft Palate Craniofac J 31(3):217–223

    Article  PubMed  CAS  Google Scholar 

  • Lamoury FM, Croitoru-Lamoury J, Brew BJ (2006) Undifferentiated mouse mesenchymal stem cells spontaneously express neural and stem cell markers Oct-4 and Rex-1. Cytotherapy 8(3):228–242

    Article  PubMed  CAS  Google Scholar 

  • Langer HF, Stellos K, Steingen C, Froihofer A, Schonberger T, Kramer B, Bigalke B, May AE, Seizer P, Muller I, Gieseke F, Siegel-Axel D, Meuth SG, Schmidt A, Wendel HP, Muller I, Bloch W, Gawaz M (2009) Platelet derived bFGF mediates vascular integrative mechanisms of mesenchymal stem cells in vitro. J Mol Cell Cardiol 47(2):315–325

    Article  PubMed  CAS  Google Scholar 

  • Leucht P, Kim JB, Amasha R, James AW, Girod S, Helms JA (2008) Embryonic origin and Hox status determine progenitor cell fate during adult bone regeneration. Development 135(17):2845–2854

    Article  PubMed  CAS  Google Scholar 

  • Li RK, Mickle DA, Weisel RD, Rao V, Jia ZQ (2001) Optimal time for cardiomyocyte transplantation to maximize myocardial function after left ventricular injury. Ann Thorac Surg 72(6):1957–1963

    Article  PubMed  CAS  Google Scholar 

  • Li X, Liu X, Tan Y, Tran V, Zhang N, Wen X (2012) Improve the viability of transplanted neural cells with appropriate sized neurospheres coated with mesenchymal stem cells. Med Hypotheses 79(2):274–277

    Article  PubMed  Google Scholar 

  • Matsubara T, Suardita K, Ishii M, Sugiyama M, Igarashi A, Oda R, Nishimura M, Saito M, Nakagawa K, Yamanaka K, Miyazaki K, Shimizu M, Bhawal UK, Tsuji K, Nakamura K, Kato Y (2005) Alveolar bone marrow as a cell source for regenerative medicine: differences between alveolar and iliac bone marrow stromal cells. J Bone Miner Res 20(3):399–409

    Article  PubMed  CAS  Google Scholar 

  • Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B, Sadoshima J (2007) Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res 100:914–922

  • Millman JR, Tan JH, Colton CK (2009) The effects of low oxygen on self-renewal and differentiation of embryonic stem cells. Curr Opin Organ Transplant 14(6):694–700

    Article  PubMed  Google Scholar 

  • Nie H, Lee CH, Tan J, Lu C, Mendelson A, Chen M, Embree MC, Kong K, Shah B, Wang S, Cho S, Mao JJ (2012) Musculoskeletal tissue engineering by endogenous stem/progenitor cells. Cell Tissue Res 347(3):665–676

    Article  PubMed  CAS  Google Scholar 

  • Pan H, Cai N, Li M, Liu GH, Izpisua BJ (2013) Autophagic control of cell ‘stemness’. EMBO Mol Med 5(3):327–331

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Phadwal K, Watson AS, Simon AK (2013) Tightrope act: autophagy in stem cell renewal, differentiation, proliferation, and aging. Cell Mol Life Sci 70(1):89–103

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Reichert JC, Gohlke J, Friis TE, Quent VM, Hutmacher DW (2013) Mesodermal and neural crest derived ovine tibial and mandibular osteoblasts display distinct molecular differences. Gene 525(1):99–106

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Guijo FM, Blanco JF, Cruz G, Muntion S, Gomez M, Carrancio S, Lopez-Villar O, Barbado MV, Sanchez-Abarca LI, Blanco B, Brinon JG, Del CM (2009) Multiparametric comparison of mesenchymal stromal cells obtained from trabecular bone by using a novel isolation method with those obtained by iliac crest aspiration from the same subjects. Cell Tissue Res 336(3):501–507

    Article  PubMed  Google Scholar 

  • Siddappa R, Fernandes H, Liu J, van Blitterswijk C, de Boer J (2007) The response of human mesenchymal stem cells to osteogenic signals and its impact on bone tissue engineering. Curr Stem Cell Res Ther 2(3):209–220

    Article  PubMed  CAS  Google Scholar 

  • Wang F, Thirumangalathu S, Loeken MR (2006) Establishment of new mouse embryonic stem cell lines is improved by physiological glucose and oxygen. Cloning Stem Cells 8(2):108–116

    Article  PubMed  CAS  Google Scholar 

  • Watanabe N, Takai S, Morita N, Kawata M, Hirasawa Y (1999) A method of tracking donor cells after simulated autologous transplantation: a study using synovial cells of transgenic rats. Cell Tissue Res 298(3):519–525

    Article  PubMed  CAS  Google Scholar 

  • Wheeler DL, Eschbach EJ, Hoellrich RG, Montfort MJ, Chamberland DL (2000) Assessment of resorbable bioactive material for grafting of critical-size cancellous defects. J Orthop Res 18(1):140–148

    Article  PubMed  CAS  Google Scholar 

  • Yamaza T, Ren G, Akiyama K, Chen C, Shi Y, Shi S (2011) Mouse mandible contains distinctive mesenchymal stem cells. J Dent Res 90(3):317–324

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yoshimura H, Muneta T, Nimura A, Yokoyama A, Koga H, Sekiya I (2007) Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res 327:449–462

  • Zhang P, Men J, Fu Y, Shan T, Ye J, Wu Y, Tao Z, Liu L, Jiang H (2012) Contribution of SATB2 to the stronger osteogenic potential of bone marrow stromal cells from craniofacial bones. Cell Tissue Res 350(3):425–437

    Article  PubMed  CAS  Google Scholar 

  • Zhu W, Chen J, Cong X, Hu S, Chen X (2006) Hypoxia and serum deprivation-induced apoptosis in mesenchymal stem cells. Stem Cells 24(2):416–425

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a National Natural Science Foundation of China grant (81070810) and is a project funded by the Priority Academic Program for the Development of Jiangsu Higher Education Institutions.

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Correspondence to Hongbing Jiang.

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Dong, W., Ge, J., Zhang, P. et al. Phenotypic characterization of craniofacial bone marrow stromal cells: unique properties of enhanced osteogenesis, cell recruitment, autophagy, and apoptosis resistance. Cell Tissue Res 358, 165–175 (2014). https://doi.org/10.1007/s00441-014-1927-4

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  • DOI: https://doi.org/10.1007/s00441-014-1927-4

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