Expresión de Runx2 en Células Mesenquimáticas de la Membrana del Seno Maxilar y el Periostio Asociado

Implicancias Para la Osteogénesis en Procedimientos de Elevación Sinusal

Autores/as

DOI:

https://doi.org/10.62172/revfouba.n98.a328

Palabras clave:

membrana sinusal, membrana de Schneider, células mesenquimáticas, Runx2, osteogénesis

Resumen

El objetivo de este estudio fue evidenciar, mediante la expresión del factor de transcripción Runx2, la presencia de células mesenquimáticas con capacidad de diferenciación hacia el linaje osteoprogenitor en la membrana de Schneider y el periostio asociado del seno maxilar. Se procesaron histológicamente los maxilares superiores de ratas Wistar macho de 7 semanas de edad, y sobre cortes coronales a la altura de los primeros molares superiores se realizaron tinciones con hematoxilina-eosina y tricrómico de Masson, e inmunomarcación para Runx2. Se realizó el análisis histológico de la mucosa del seno maxilar identificando células mesenquimáticas según criterios morfológicos y complementando su caracterización con la expresión nuclear de Runx2. En la lámina propia de la membrana de Schneider y en la capa interna del periostio asociado se identificaron numerosas células de morfología mesenquimática, dispuestas de manera difusa en el estroma subepitelial y con mayor densidad perivascular. La inmunomarcación reveló positividad nuclear para Runx2 en una subpoblación de estas células tanto en la lámina propia como en el periostio, con un patrón más constante en este último, mientras que el epitelio respiratorio y la capa fibrosa externa resultaron negativos. Estos hallazgos demuestran in vivo la presencia y localización de células mesenquimáticas con compromiso osteogénico en la membrana de Schneider y el periostio adyacente, aportando sustento biológico a la posible participación de la membrana sinusal en los procesos de regeneración ósea observados tras la elevación del seno maxilar.

Citas

Ari, I., Karaca, Ç., Er, N., y Ocak, M. (2024). Effects of sinus membrane stabilization by dental implant placement and membrane suturing on endo-sinus bone gain in cases of lateral sinus elevation performed without graft material. The International Journal of Oral & Maxillofacial Implants, 39(4), 585–594. https://doi.org/10.11607/jomi.10700

Bassi, A. P. F., Pioto, R., Faverani, L. P., Canestraro, D., y Fontão, F. G. K. (2015). Maxillary sinus lift without grafting, and simultaneous implant placement: a prospective clinical study with a 51-month follow-up. International Journal of Oral and Maxillofacial Surgery, 44(7), 902–907. https://doi.org/10.1016/j.ijom.2015.03.016

Berbéri, A., Al-Nemer, F., Hamade, E., Noujeim, Z., Badran, B., y Zibara, K. (2017). Mesenchymal stem cells with osteogenic potential in human maxillary sinus membrane: an in vitro study. Clinical Oral Investigations, 21(5), 1599–1609. https://doi.org/10.1007/s00784-016-1945-6

Bianco, P., y Robey, P. G. (2015). Skeletal stem cells. Development, 142(6), 1023–1027. https://doi.org/10.1242/dev.102210

Borges, F. L., Dias, R. O., Piattelli, A., Onuma, T., Cardoso, L. A. G., Salomão, M., Scarano, A., Ayub, E., y Shibli, J. A. (2011). Simultaneous sinus membrane elevation and dental implant placement without bone graft: a 6-month follow-up study. Journal of Periodontology, 82(3), 403–412. https://doi.org/10.1902/jop.2010.100343

Chen, T. W., Chang, H. S., Leung, K. W., Lai, Y. L., y Kao, S. Y. (2007). Implant placement immediately after the lateral approach of the trap door window procedure to create a maxillary sinus lift without bone grafting: a 2-year retrospective evaluation of 47 implants in 33 patients. Journal of Oral and Maxillofacial Surgery, 65(11), 2324–2328. https://doi.org/10.1016/j.joms.2007.06.649

Choi, Y., Lee, J. S., Kim, Y. J., Kim, M. S., Choi, S. H., Cho, K. S., y Jung, U. W. (2013). Recombinant human bone morphogenetic protein-2 stimulates the osteogenic potential of the Schneiderian membrane: a histometric analysis in rabbits. Tissue Engineering. Part A, 19(17-18), 1994–2004. https://doi.org/10.1089/ten.TEA.2012.0724

Cricchio, G., Palma, V. C., Faria, P. E., de Oliveira, J. A., Lundgren, S., Sennerby, L., y Salata, L. A. (2009). Histological findings following the use of a space-making device for bone reformation and implant integration in the maxillary sinus of primates. Clinical Implant Dentistry and Related Research, 11(Suppl 1), e14–e22. https://doi.org/10.1111/j.1708-8208.2009.00158.x

Cricchio, G., Sennerby, L., y Lundgren, S. (2011). Sinus bone formation and implant survival after sinus membrane elevation and implant placement: a 1- to 6-year follow-up study. Clinical Oral Implants Research, 22(10), 1200–1212. https://doi.org/10.1111/j.1600-0501.2010.02096.x

Edranov, S. S., Kovalyeva, I. V., Kryukov, K. I., y Konovko, A. A. (2004). Anatomic and histological study of maxillary sinus in albino rat. Bulletin of Experimental Biology and Medicine, 138(6), 603–606. https://doi.org/10.1007/s10517-005-0137-1

Falah, M., Sohn, D. S., y Srouji, S. (2016). Graftless sinus augmentation with simultaneous dental implant placement: clinical results and biological perspectives. International Journal of Oral and Maxillofacial Surgery, 45(9), 1147–1153. https://doi.org/10.1016/j.ijom.2016.05.006

Ferretti, C., y Mattioli-Belmonte, M. (2014). Periosteum derived stem cells for regenerative medicine proposals: boosting current knowledge. World Journal of Stem Cells, 6(3), 266–277. https://doi.org/10.4252/wjsc.v6.i3.266

Friedenstein, A. J., Chailakhyan, R. K., y Gerasimov, U. V. (1987). Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell and Tissue Kinetics, 20(3), 263–272. https://doi.org/10.1111/j.1365-2184.1987.tb01309.x

Graziano, A., Benedetti, L., Massei, G., Cusella de Angelis, M. G., Ferrarotti, F., y Aimetti, M. (2012). Bone production by human maxillary sinus mucosa cells. Journal of Cellular Physiology, 227(9), 3278–3281. https://doi.org/10.1002/jcp.24022

Guo, J., Weng, J., Rong, Q., Zhang, X., Zhu, S., Huang, D., Li, X., y Chen, S. (2015). Investigation of multipotent postnatal stem cells from human maxillary sinus membrane. Scientific Reports, 5, 11660. https://doi.org/10.1038/srep11660

Hatano, N., Sennerby, L., y Lundgren, S. (2007). Maxillary sinus augmentation using sinus membrane elevation and peripheral venous blood for implant-supported rehabilitation of the atrophic posterior maxilla: case series. Clinical Implant Dentistry and Related Research, 9(3), 150–155. https://doi.org/10.1111/j.1708-8208.2007.00045.x

He, F., Umrath, F., Reinert, S., y Alexander, D. (2021). Jaw periosteum-derived mesenchymal stem cells regulate THP-1-derived macrophage polarization. International Journal of Molecular Sciences, 22(9), 4310. https://doi.org/10.3390/ijms22094310

Kaneko, T., Masuda, I., Horie, N., y Shimoyama, T. (2012). New bone formation in nongrafted sinus lifting with space-maintaining management: a novel technique using a titanium bone fixation device. Journal of Oral and Maxillofacial Surgery, 70(3), e217–e224. https://doi.org/10.1016/j.joms.2011.10.025

Lian, J. B., Javed, A., Zaidi, S. K., Lengner, C., Montecino, M., van Wijnen, A. J., Stein, J. L., y Stein, G. S. (2004). Regulatory controls for osteoblast growth and differentiation: role of Runx/Cbfa/AML factors. Critical Reviews in Eukaryotic Gene Expression, 14(1-2), 1–41. http://www.begellhouse.com/journals/6dbf508d3b17c437,3b6cf6f002e9c0d3,0ca17b26280cf883.html

Lie, N., Merten, H.-A., Meyns, J., Lethaus, B., Wiltfang, J., y Kessler, P. (2015). Elevation of the maxillary sinus membrane for de-novo bone formation: first results of a prospective study in humans. Journal of Cranio-Maxillofacial Surgery, 43(8), 1670–1677. https://doi.org/10.1016/j.jcms.2015.07.011

Lin, I. C., Gonzalez, A. M., Chang, H. J., Kao, S. Y., y Chen, T. W. (2011). A 5-year follow-up of 80 implants in 44 patients placed immediately after the lateral trap-door window procedure to accomplish maxillary sinus elevation without bone grafting. The International Journal of Oral & Maxillofacial Implants, 26(5), 1079–1086. https://www.quintessence-publishing.com/usa/en/article/845799

Lundgren, S., Andersson, S., y Sennerby, L. (2003). Spontaneous bone formation in the maxillary sinus after removal of a cyst: coincidence or consequence? Clinical Implant Dentistry and Related Research, 5(2), 78–81. https://doi.org/10.1111/j.1708-8208.2003.tb00187.x

Lundgren, S., Cricchio, G., Palma, V. C., Salata, L. A., y Sennerby, L. (2008). Sinus membrane elevation and simultaneous insertion of dental implants: a new surgical technique in maxillary sinus floor augmentation. Periodontology 2000, 47(1), 193–205. https://doi.org/10.1111/j.1600-0757.2008.00264.x

Lundgren, S., Cricchio, G., Hallman, M., Jungner, M., Rasmusson, L., y Sennerby, L. (2017). Sinus floor elevation procedures to enable implant placement and integration: techniques, biological aspects and clinical outcomes. Periodontology 2000, 73(1), 103–120. https://doi.org/10.1111/prd.12165

Lundgren, S., Johansson, A. S., Cricchio, G., y Lundgren, S. (2019). Clinical outcome and factors determining new bone formation in lateral sinus membrane elevation with simultaneous implant placement without grafting material: a cross-sectional, 3-17 year follow-up study. Clinical Implant Dentistry and Related Research, 21(5), 827–834. https://doi.org/10.1111/cid.12758

Mangano, F. G., Colombo, M., Veronesi, G., Caprioglio, A., y Mangano, C. (2015). Mesenchymal stem cells in maxillary sinus augmentation: a systematic review with meta-analysis. World Journal of Stem Cells, 7(6), 976–991. https://doi.org/10.4252/wjsc.v7.i6.976

Marolt, D., Knezevic, M., y Vunjak-Novakovic, G. (2010). Bone tissue engineering with human stem cells. Stem Cell Research & Therapy, 1(2), 10. https://doi.org/10.1186/scrt10

National Research Council. (2011). Guide for the Care and Use of Laboratory Animals [en línea]. (8va. ed.). National Academies Press. https://doi.org/10.17226/12910

Palma, V. C., Magro-Filho, O., de Oliveira, J. A., Lundgren, S., Salata, L. A., y Sennerby, L. (2006). Bone reformation and implant integration following maxillary sinus membrane elevation: an experimental study in primates. Clinical Implant Dentistry and Related Research, 8(1), 11–24. https://doi.org/10.2310/6480.2005.00026.x

Patro, B. P., Rath, M., Mohapatra, D., Kumar Patra, S., Chandra Sahu, M., Das, G., y Sahoo, J. (2021). Traumatized periosteum: its histology, viability, and clinical significance. Orthopedic Reviews, 14(1), 30044. https://doi.org/10.52965/001c.30044

Peng, W., Zhu, S. X., Wang, J., Chen, L. L., Weng, J. Q., y Chen, S. L. (2018). Lnc-NTF3-5 promotes osteogenic differentiation of maxillary sinus membrane stem cells via sponging miR-93-3p. Clinical Implant Dentistry and Related Research, 20(2), 110–121. https://doi.org/10.1111/cid.12553

Peng, W., Zhu, S., Chen, J., Wang, J., Rong, Q., y Chen, S. (2019). Hsa_circRNA_33287 promotes the osteogenic differentiation of maxillary sinus membrane stem cells via miR-214-3p/Runx3. Biomedicine & Pharmacotherapy, 109, 1709–1717. https://doi.org/10.1016/j.biopha.2018.10.159

Ramirez, J. M., Bai, Q., Dijon-Grinand, M., Assou, S., Gerbal-Chaloin, S., Hamamah, S., y De Vos, J. (2010). Human pluripotent stem cells: from biology to cell therapy. World Journal of Stem Cells, 2(2), 24–33. https://doi.org/10.4252/wjsc.v2.i2.24

Razzouk, S., y Schoor, R. (2012). Mesenchymal stem cells and their challenges for bone regeneration and osseointegration. Journal of Periodontology, 83(5), 547–550. https://doi.org/10.1902/jop.2011.110384

Ren, J., Geng, N., Xia, Y., Zhou, Y., Tan, J., Peng, W., y Chen, S. (2022). A comparative study of the morphology and molecular biology between the Schneiderian membrane and palatine mucoperiosteum. Tissue and Cell, 79, 101948. https://doi.org/10.1016/j.tice.2022.101948

Riben, C., y Thor, A. (2016). Follow‐up of the sinus membrane elevation technique for maxillary sinus implants without the use of graft material. Clinical Implant Dentistry and Related Research, 18(5), 895–905. https://doi.org/10.1111/cid.12360

Rong, Q., Li, X., Chen, S. L., Zhu, S. X., y Huang, D. Y. (2015). Effect of the Schneiderian membrane on the formation of bone after lifting the floor of the maxillary sinus: an experimental study in dogs. British Journal of Oral and Maxillofacial Surgery, 53(7), 607–612. https://doi.org/10.1016/j.bjoms.2015.02.010

Si, M. S., Zhuang, L. F., Gu, Y. X., Mo, J. J., Qiao, S. C., y Lai, H. C. (2013). Osteotome sinus floor elevation with or without grafting: a 3-year randomized controlled clinical trial. Journal of Clinical Periodontology, 40(4), 396–403. https://doi.org/10.1111/jcpe.12066

Sohn, D. S., Lee, J. S., Ahn, M. R., y Shin, H. I. (2008). New bone formation in the maxillary sinus without bone grafts. Implant Dentistry, 17(3), 321–331. https://doi.org/10.1097/ID.0b013e318182f01b

Sohn, D. S., Moon, J. W., Lee, W. H., Kim, S. S., Kim, C. W., Kim, K. T., y Moon, Y. S. (2011). Comparison of new bone formation in the maxillary sinus with and without bone grafts: immunochemical rabbit study. The International Journal of Oral & Maxillofacial Implants, 26(5), 1033–1042. https://www.quintessence-publishing.com/usa/en/article/845794/

Srouji, S., Kizhner, T., Ben David, D., Riminucci, M., Bianco, P., y Livne, E. (2009). The Schneiderian membrane contains osteoprogenitor cells: in vivo and in vitro study. Calcified Tissue International, 84(2), 138–145. https://doi.org/10.1007/s00223-008-9202-x

Srouji, S., Ben-David, D., Lotan, R., Riminucci, M., Livne, E., y Bianco, P. (2010). The innate osteogenic potential of the maxillary sinus (Schneiderian) membrane: an ectopic tissue transplant model simulating sinus lifting. International Journal of Oral and Maxillofacial Surgery, 39(8), 793–801. https://doi.org/10.1016/j.ijom.2010.03.009

Thor, A., Sennerby, L., Hirsch, J. M., y Rasmusson, L. (2007). Bone formation at the maxillary sinus floor following simultaneous elevation of the mucosal lining and implant installation without graft material: an evaluation of 20 patients treated with 44 Astra Tech implants. Journal of Oral and Maxillofacial Surgery, 65(7 Suppl 1), 64–72. https://doi.org/10.1016/j.joms.2006.10.047

Vimalraj, S., Arumugam, B., Miranda, P. J., y Selvamurugan, N. (2015). Runx2: Structure, function, and phosphorylation in osteoblast differentiation. International Journal of Biological Macromolecules, 78, 202–208. https://doi.org/10.1016/j.ijbiomac.2015.04.008

Weng, J., Peng, W., Zhu, S., y Chen, S. (2017). Long noncoding RNA sponges miR-454 to promote osteogenic differentiation in maxillary sinus membrane stem cells. Implant Dentistry, 26(2), 178–186. https://doi.org/10.1097/ID.0000000000000569

Xu, J., Li, Z., Hou, Y., y Fang, W. (2015). Potential mechanisms underlying the Runx2 induced osteogenesis of bone marrow mesenchymal stem cells. American Journal of Translational Research, 7(12), 2527–2535. https://pmc.ncbi.nlm.nih.gov/articles/pmid/26885254/

Yun, K. I., Kim, D. J., y Park, J. U. (2013). Osteogenic potential of adult stem cells from human maxillary sinus membrane by Simvastatin in vitro: preliminary report. Journal of the Korean Association of Oral and Maxillofacial Surgeons, 39(4), 150–155. https://doi.org/10.5125/jkaoms.2013.39.4.150

Zhu, S., Chen, W., Masson, A., y Li, Y. P. (2024). Cell signaling and transcriptional regulation of osteoblast lineage commitment, differentiation, bone formation, and homeostasis. Cell Discovery, 10(1), 71. https://doi.org/10.1038/s41421-024-00689-6

Descargas

Publicado

2026-08-03

Cómo citar

Vila, M. C., Puia, S., De Lucca, R. C., & Bozal, C. (2026). Expresión de Runx2 en Células Mesenquimáticas de la Membrana del Seno Maxilar y el Periostio Asociado: Implicancias Para la Osteogénesis en Procedimientos de Elevación Sinusal. Revista De La Facultad De Odontologia. Universidad De Buenos Aires, 41(98). https://doi.org/10.62172/revfouba.n98.a328