Research Article
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Osteogenic differentiation of canine adipose derived mesenchymal stem cells on B‐TCP and B‐TCP/Collagen biomaterials

Year 2024, , 125 - 134, 01.04.2024

Özge Özgenç , Asuman Özen

https://doi.org/10.33988/auvfd.1130705
Cited By: 1

Abstract

Mesenchymal stem cells are adult stem cells that can differentiate into osteogenic, chondrogenic, adipogenic and myogenic lineages. In orthopedics and traumatology, mesenchymal stem cells, combined with biomaterials, are used mainly for treating bone fractures and diseases in humans and animals. This study aims to promote the growth, proliferation, and osteogenic differentiation of mesenchymal stem cells isolated from the adipose tissue of canines on B‐TCP (Beta‐tricalcium phosphate) and B‐TCP/Collagen biomaterials. MTT analysis was performed to test the cell adhesion and proliferation on B‐TCP and B‐TCP/Collagen biomaterials used to mimic the extracellular matrix of three‐dimensional bone tissue. Scanning electron microscope analysis was performed to show general surface characters of BTCP and B‐TCP /Collagen biomaterials. The osteoinductive capacities of the BTCP and B‐TCP/Collagen biomaterials were determined by alkaline phosphatase and Von Kossa stainings, and RT‐PCR analysis. The ALP activity of the B‐TCP/Col containing material was significantly higher than the B‐TCP in the early days. In terms of gene expression, there were no significant differences except 14thday SPARC gene expression. The results of Von Kossa staining indicated that BTCP/ Col has above the desired level degradation capacity. As a result of this
research, although it is advantageous in terms of alkaline phosphatase activity and osteogenic gene expression compared to B‐TCP material, it is thought that B‐TCP/Collagen biomaterial should be developed for use in bone tissue engineering due to its high degradation property.

Keywords

Adipose tissue biomaterial canine mesenchymal stem cell osteogenic differentiation.

Ethical Statement

This study was approved by Ankara University Animal Experiments Local Ethics Committee (2017-5-37).

Supporting Institution

This research was funded by Ankara University Scientific Research Projects Coordination (project number 17L0239015).

Project Number

17L0239015

Thanks

The authors would like to thank Açelya Yılmazer Aktuna and Ezgi İrem Bektaş Taş for their support and BMT Calsis for providing biomaterials. This study was produced from the PhD thesis of the first author.

References

  • Arahira T, Todo M (2016): Variation of mechanical behavior of β-TCP/collagen two phase composite scaffold with mesenchymal stem cell in vitro. J Mech Behav Biomed Mater, 61, 464-474.
  • Assaf RB, Fayyad-Kazan M, Al-Nemer F, et al (2019): Evaluation of the osteogenic potential of different scaffolds embedded with human stem cells originated from schneiderian membrane: An in vitro study. Biomed Res Int, 2019, 1-10.
  • Bose S, Roy M, Bandyopadhyay A (2012): Recent advances in bone tissue engineering scaffolds. Trends Biotechnol, 30, 546-554.
  • Brokesh AM, Gaharwar AK (2020): Inorganic biomaterials for regenerative medicine. ACS Appl Mater Interfaces, 12, 5319-5344.
  • Brzoska M, Geiger H, Gauer S, et al (2005): Epithelial differentiation of human adipose tissue-derived adult stem cells. Biochem Biophys Res Commun, 330, 142-150.
  • Can A (2014): Kök Hücre, Biyolojisi Türleri ve Tedavide Kullanımları. Akademisyen Kitabevi. Ankara.
  • Cao H, Kuboyama N (2010): A biodegradable porous composite scaffold of PGA/β-TCP for bone tissue engineering. Bone, 46, 386-395.
  • Caplan AI (2008) Why are MSCs therapeutic? new data: New insight. J Pathol 217, 318–324.
  • Cerci E, Erdost H (2019): Phenotypic characterization and differentiation of mesenchymal stem cells originating from adipose tissue. Turkish J Vet Anim Sci, 43, 834-845.
  • Cerci E, Erdost H (2021): Rapid, practical and safe isolation of adipose derived stem cells. Biotech Histochem, 96, 138-145.
  • Choy CS, Lee WF, Lin PY, et al (2021): Surface modified β-Tricalcium phosphate enhanced stem cell osteogenic differentiation in vitro and bone regeneration in vivo. Sci Rep, 11, 1-14.
  • Correia C, Bhumiratana S, Yan LP, et al (2012): Development of silk-based scaffolds for tissue engineering of bone from human adipose-derived stem cells. Acta Biomater, 8, 2483-2492.
  • Dai R, Wang Z, Samanipour R, et al (2016): Adiposederived stem cells for tissue engineering and regenerative medicine applications. Stem Cells Int, 2016, 1-19.
  • Deschaseaux F, Sensébé L, Heymann D (2009): Mechanisms of bone repair and regeneration. Trends Mol Med, 15, 417-429.
  • Donzelli E, Salvadè A, Mimo P, et al (2007): Mesenchymal stem cells cultured on a collagen scaffold: In vitro osteogenic differentiation. Arch Oral Biol, 52, 64-73.
  • Ebrahimi M, Botelho MG, Dorozhkin SV (2017): Biphasic calcium phosphates bioceramics (HA/TCP): concept, physicochemical properties and the impact of standardization of study protocols in biomaterials research. Mater Sci Eng C Mater Biol Appl, 71, 1293-1312.
  • Friedenstein AJ, Piatetzky SII, Petrakova KV (1966): Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol, 16, 381-390.
  • Gronthos S, Franklin DM, Leddy HA, et al (2001): Surface protein characterization of human adipose tissue derived stromal cells. J Cell Physiol, 189, 54-63.
  • Hilal A, Ece Ç, Marzieh KK, et al (2020): Histologic and electromyographic evaluation of neuroregenerative effect of stromal vascular fraction following neuroanastomosis. Kafkas Univ Vet Fak Derg, 26, 483-490.
  • Huri PY, Hasirci N, Hasirci V (2010): Kemik doku mühendisliği. AKTD, 19, 206-219.
  • Jurgens WJ, Oedayrajsingh-Varma MJ, Helder MN, et al (2008): Effect of tissue-harvesting site on yield of stem cells derived from adipose tissue: implications for cellbased therapies. Cell Tissue Res, 332, 415-426.
  • Karadzic I, Vucic V, Jokanovic V, et al (2015): Effects of novel hydroxyapatite based 3D biomaterials on proliferation and osteoblastic differentiation of mesenchymal stem cells. J Biomed Mater Res A, 103, 350-357.
  • Kato E, Lemler J, Sakurai K, et al (2014): Biodegradation property of Beta‐Tricalcium Phosphate‐Collagen composite in accordance with bone formation: a comparative study with Bio‐Oss Collagen® in a rat critical‐size defect model. Clin Implant Dent Relat Res, 16, 202-211.
  • Komori T (2005): Regulation of skeletal development by the Runx family of transcription factors. J Cell Biochem, 95, 445-453.
  • Li WJ, Tuli R, Huang X, et al (2005): Multilineage differentiation of human mesenchymal stem cells in a threedimensional nanofibrous scaffold. Biomaterials, 25, 5158-5166.
  • Malafaya PB, Silva GA, Reis RL (2007): Natural-origin polymers as carriers and scaffolds for biomolecules and cell delivery in tissue engineering applications. Adv Drug Deliv Rev, 59, 207-233.
  • Martinello T, Bronzini I, Maccatrozzo L, et al (2011): Canine adipose-derived-mesenchymal stem cells do not lose stem features after a long-term cryopreservation. Res Vet Sci, 91, 18-24.
  • Marx C, Silveira MD, Beyer Nardi N (2015): Adiposederived stem cells in veterinary medicine: characterization and therapeutic applications. Stem Cells Dev, 24, 803-813.
  • Morikawa S, Yo M, Yoshiaki K, et al (2009): Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. Exp Med, 206, 2483-2496.
  • Mravic M, Péault B, James AW (2014): Current trends in bone tissue engineering. Biomed Res Int, 2014, 1-5.
  • Mygind T, Stiehler M, Baatrup A, et al (2007): Mesenchymal stem cell ingrowth and differentiation on coralline hydroxyapatite scaffolds. Biomaterials, 28, 1036-1047.
  • Ozdal Kurt F, Tuğlu I, Vatansever H, et al (2016): The effect of different implant biomaterials on the behavior of canine bone marrow stromal cells during their differentiation into osteoblasts. Biotech Histochem, 91, 412-422.
  • Ozen A, Sancak IG, Ceylan A, et al (2016): Isolation of adipose tissue-derived stem cells. Turk J Vet Anim Sci, 40, 137-141.
  • Rad MR, Fahimipour F, Dashtimoghadam E, et al (2021): Osteogenic differentiation of adipose-derived mesenchymal stem cells using 3D-Printed PDLLA/β-TCP nanocomposite scaffolds. Bioprinting, 21, 1-9.
  • Rai B, Lin JL, Lim ZX, et al (2010): Differences between in vitro viability and differentiation and in vivo boneforming efficacy of human mesenchymal stem cells cultured on PCL–TCP scaffolds. Biomaterials, 31, 7960-7970.
  • Rodrigues CVM, Serricella P, Linhares ABR, et al (2014): Adipose mesenchymal stem cells in the field of bone tissue engineering. World J Stem Cells, 6, 144-152.
  • Romanov YA, Darevskaya AN, Merzlikina NV, et al (2005): Mesenchymal stem cells from human bone marrow and adipose tissue: isolation, characterization, and differentiation potentialities. Bull Exp Biol Med, 140, 138-143.
  • Rosset EM, Bradshaw AD (2016): SPARC/osteonectin in mineralized tissue. Matrix Biol, 52, 78-87.
  • Rossi MA, Duarte MEL, Farina M (2003): Characterization of a bovine collagen-hydroxyapatite composite scaffold for bone tissue engineering. Biomaterials, 24, 4987-4997.
  • Sándor GK (2012): Tissue engineering of bone: Clinical observations with adipose-derived stem cells, resorbable scaffolds, and growth factors. Ann Maxillofac Surg, 2, 8-11.
  • Sarikaya B, Aydin HM (2015): Collagen/beta-tricalcium phosphate based synthetic bone grafts via dehydrothermal processing. Biomed Res Int, 2015, 1-10.
  • Schäffler A, Büchler C (2007): Concise review: adipose tissue derived stromal cells basic and clinical implications for novel cell based therapies. Stem Cells, 25, 818-827.
  • Screven R, Kenyon E, Myers MJ, et al (2014): Immunophenotype and gene expression profile of mesenchymal stem cells derived from canine adipose tissue and bone marrow. Vet Immunol Immunopathol, 161, 21-31.
  • Seo JP, Tsuzuki N, Haneda S, et al (2012): Proliferation of equine bone marrow-derived mesenchymal stem cells in gelatin/β-tricalcium phosphate sponges. Res Vet Sci, 93, 1481-1486.
  • Song WJ, Li Q, Ryu MO, et al (2019): Canine adipose tissue-derived mesenchymal stem cells pre-treated with TNF-alpha enhance immunomodulatory effects in inflammatory bowel disease in mice. Res Vet Sci, 125, 176-184.
  • Takahashi Y, Yamamoto M, Tabata Y (2005): Osteogenic differentiation of mesenchymal stem cells in biodegradable sponges composed of gelatin and β- tricalcium phosphate. Biomaterials, 26, 3587-3596.
  • Via AG, Frizziero A, Oliva F (2012): Biological properties of mesenchymal stem cells from different sources. MLTJ, 2, 154.
  • Vieira NM, Brandalise V, Zucconi E, et al (2010): Isolation, characterization, and differentiation potential of canine adipose-derived stem cells. Cell Transplant, 19, 279-289.
  • Villatoro AJ, Fernández V, Claros S, et al (2015): Use of adipose-derived mesenchymal stem cells in keratoconjunctivitis sicca in a canine model. Biomed Res Int, 2015, 2-4.
  • Westhauser F, Karadjian M, Essers C, et al (2019): Osteogenic differentiation of mesenchymal stem cells is enhanced in a 45S5-supplemented β-TCP composite scaffold: an in-vitro comparison of Vitoss and Vitoss BA. PloS One, 14, 1-18.
  • Wilson A, Chee M, Butler P, et al (2019): Isolation and characterisation of human adipose-derived stem cells. Methods Mol Biol, 2019, 3-13.
  • Xiaoming L, Haifeng L, Niu X, et al (2011): Osteogenic differentiation of human adipose‐derived stem cells induced by osteoinductive calcium phosphate ceramics. J Biomed Mater Res B Appl Biomater, 1, 10-19.
  • Zuk PA, Zhu M, Mizuno H, et al (2001): Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng, 7, 211-228.

Year 2024, , 125 - 134, 01.04.2024

Özge Özgenç , Asuman Özen

https://doi.org/10.33988/auvfd.1130705
Cited By: 1

Abstract

Project Number

17L0239015

References

  • Arahira T, Todo M (2016): Variation of mechanical behavior of β-TCP/collagen two phase composite scaffold with mesenchymal stem cell in vitro. J Mech Behav Biomed Mater, 61, 464-474.
  • Assaf RB, Fayyad-Kazan M, Al-Nemer F, et al (2019): Evaluation of the osteogenic potential of different scaffolds embedded with human stem cells originated from schneiderian membrane: An in vitro study. Biomed Res Int, 2019, 1-10.
  • Bose S, Roy M, Bandyopadhyay A (2012): Recent advances in bone tissue engineering scaffolds. Trends Biotechnol, 30, 546-554.
  • Brokesh AM, Gaharwar AK (2020): Inorganic biomaterials for regenerative medicine. ACS Appl Mater Interfaces, 12, 5319-5344.
  • Brzoska M, Geiger H, Gauer S, et al (2005): Epithelial differentiation of human adipose tissue-derived adult stem cells. Biochem Biophys Res Commun, 330, 142-150.
  • Can A (2014): Kök Hücre, Biyolojisi Türleri ve Tedavide Kullanımları. Akademisyen Kitabevi. Ankara.
  • Cao H, Kuboyama N (2010): A biodegradable porous composite scaffold of PGA/β-TCP for bone tissue engineering. Bone, 46, 386-395.
  • Caplan AI (2008) Why are MSCs therapeutic? new data: New insight. J Pathol 217, 318–324.
  • Cerci E, Erdost H (2019): Phenotypic characterization and differentiation of mesenchymal stem cells originating from adipose tissue. Turkish J Vet Anim Sci, 43, 834-845.
  • Cerci E, Erdost H (2021): Rapid, practical and safe isolation of adipose derived stem cells. Biotech Histochem, 96, 138-145.
  • Choy CS, Lee WF, Lin PY, et al (2021): Surface modified β-Tricalcium phosphate enhanced stem cell osteogenic differentiation in vitro and bone regeneration in vivo. Sci Rep, 11, 1-14.
  • Correia C, Bhumiratana S, Yan LP, et al (2012): Development of silk-based scaffolds for tissue engineering of bone from human adipose-derived stem cells. Acta Biomater, 8, 2483-2492.
  • Dai R, Wang Z, Samanipour R, et al (2016): Adiposederived stem cells for tissue engineering and regenerative medicine applications. Stem Cells Int, 2016, 1-19.
  • Deschaseaux F, Sensébé L, Heymann D (2009): Mechanisms of bone repair and regeneration. Trends Mol Med, 15, 417-429.
  • Donzelli E, Salvadè A, Mimo P, et al (2007): Mesenchymal stem cells cultured on a collagen scaffold: In vitro osteogenic differentiation. Arch Oral Biol, 52, 64-73.
  • Ebrahimi M, Botelho MG, Dorozhkin SV (2017): Biphasic calcium phosphates bioceramics (HA/TCP): concept, physicochemical properties and the impact of standardization of study protocols in biomaterials research. Mater Sci Eng C Mater Biol Appl, 71, 1293-1312.
  • Friedenstein AJ, Piatetzky SII, Petrakova KV (1966): Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol, 16, 381-390.
  • Gronthos S, Franklin DM, Leddy HA, et al (2001): Surface protein characterization of human adipose tissue derived stromal cells. J Cell Physiol, 189, 54-63.
  • Hilal A, Ece Ç, Marzieh KK, et al (2020): Histologic and electromyographic evaluation of neuroregenerative effect of stromal vascular fraction following neuroanastomosis. Kafkas Univ Vet Fak Derg, 26, 483-490.
  • Huri PY, Hasirci N, Hasirci V (2010): Kemik doku mühendisliği. AKTD, 19, 206-219.
  • Jurgens WJ, Oedayrajsingh-Varma MJ, Helder MN, et al (2008): Effect of tissue-harvesting site on yield of stem cells derived from adipose tissue: implications for cellbased therapies. Cell Tissue Res, 332, 415-426.
  • Karadzic I, Vucic V, Jokanovic V, et al (2015): Effects of novel hydroxyapatite based 3D biomaterials on proliferation and osteoblastic differentiation of mesenchymal stem cells. J Biomed Mater Res A, 103, 350-357.
  • Kato E, Lemler J, Sakurai K, et al (2014): Biodegradation property of Beta‐Tricalcium Phosphate‐Collagen composite in accordance with bone formation: a comparative study with Bio‐Oss Collagen® in a rat critical‐size defect model. Clin Implant Dent Relat Res, 16, 202-211.
  • Komori T (2005): Regulation of skeletal development by the Runx family of transcription factors. J Cell Biochem, 95, 445-453.
  • Li WJ, Tuli R, Huang X, et al (2005): Multilineage differentiation of human mesenchymal stem cells in a threedimensional nanofibrous scaffold. Biomaterials, 25, 5158-5166.
  • Malafaya PB, Silva GA, Reis RL (2007): Natural-origin polymers as carriers and scaffolds for biomolecules and cell delivery in tissue engineering applications. Adv Drug Deliv Rev, 59, 207-233.
  • Martinello T, Bronzini I, Maccatrozzo L, et al (2011): Canine adipose-derived-mesenchymal stem cells do not lose stem features after a long-term cryopreservation. Res Vet Sci, 91, 18-24.
  • Marx C, Silveira MD, Beyer Nardi N (2015): Adiposederived stem cells in veterinary medicine: characterization and therapeutic applications. Stem Cells Dev, 24, 803-813.
  • Morikawa S, Yo M, Yoshiaki K, et al (2009): Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. Exp Med, 206, 2483-2496.
  • Mravic M, Péault B, James AW (2014): Current trends in bone tissue engineering. Biomed Res Int, 2014, 1-5.
  • Mygind T, Stiehler M, Baatrup A, et al (2007): Mesenchymal stem cell ingrowth and differentiation on coralline hydroxyapatite scaffolds. Biomaterials, 28, 1036-1047.
  • Ozdal Kurt F, Tuğlu I, Vatansever H, et al (2016): The effect of different implant biomaterials on the behavior of canine bone marrow stromal cells during their differentiation into osteoblasts. Biotech Histochem, 91, 412-422.
  • Ozen A, Sancak IG, Ceylan A, et al (2016): Isolation of adipose tissue-derived stem cells. Turk J Vet Anim Sci, 40, 137-141.
  • Rad MR, Fahimipour F, Dashtimoghadam E, et al (2021): Osteogenic differentiation of adipose-derived mesenchymal stem cells using 3D-Printed PDLLA/β-TCP nanocomposite scaffolds. Bioprinting, 21, 1-9.
  • Rai B, Lin JL, Lim ZX, et al (2010): Differences between in vitro viability and differentiation and in vivo boneforming efficacy of human mesenchymal stem cells cultured on PCL–TCP scaffolds. Biomaterials, 31, 7960-7970.
  • Rodrigues CVM, Serricella P, Linhares ABR, et al (2014): Adipose mesenchymal stem cells in the field of bone tissue engineering. World J Stem Cells, 6, 144-152.
  • Romanov YA, Darevskaya AN, Merzlikina NV, et al (2005): Mesenchymal stem cells from human bone marrow and adipose tissue: isolation, characterization, and differentiation potentialities. Bull Exp Biol Med, 140, 138-143.
  • Rosset EM, Bradshaw AD (2016): SPARC/osteonectin in mineralized tissue. Matrix Biol, 52, 78-87.
  • Rossi MA, Duarte MEL, Farina M (2003): Characterization of a bovine collagen-hydroxyapatite composite scaffold for bone tissue engineering. Biomaterials, 24, 4987-4997.
  • Sándor GK (2012): Tissue engineering of bone: Clinical observations with adipose-derived stem cells, resorbable scaffolds, and growth factors. Ann Maxillofac Surg, 2, 8-11.
  • Sarikaya B, Aydin HM (2015): Collagen/beta-tricalcium phosphate based synthetic bone grafts via dehydrothermal processing. Biomed Res Int, 2015, 1-10.
  • Schäffler A, Büchler C (2007): Concise review: adipose tissue derived stromal cells basic and clinical implications for novel cell based therapies. Stem Cells, 25, 818-827.
  • Screven R, Kenyon E, Myers MJ, et al (2014): Immunophenotype and gene expression profile of mesenchymal stem cells derived from canine adipose tissue and bone marrow. Vet Immunol Immunopathol, 161, 21-31.
  • Seo JP, Tsuzuki N, Haneda S, et al (2012): Proliferation of equine bone marrow-derived mesenchymal stem cells in gelatin/β-tricalcium phosphate sponges. Res Vet Sci, 93, 1481-1486.
  • Song WJ, Li Q, Ryu MO, et al (2019): Canine adipose tissue-derived mesenchymal stem cells pre-treated with TNF-alpha enhance immunomodulatory effects in inflammatory bowel disease in mice. Res Vet Sci, 125, 176-184.
  • Takahashi Y, Yamamoto M, Tabata Y (2005): Osteogenic differentiation of mesenchymal stem cells in biodegradable sponges composed of gelatin and β- tricalcium phosphate. Biomaterials, 26, 3587-3596.
  • Via AG, Frizziero A, Oliva F (2012): Biological properties of mesenchymal stem cells from different sources. MLTJ, 2, 154.
  • Vieira NM, Brandalise V, Zucconi E, et al (2010): Isolation, characterization, and differentiation potential of canine adipose-derived stem cells. Cell Transplant, 19, 279-289.
  • Villatoro AJ, Fernández V, Claros S, et al (2015): Use of adipose-derived mesenchymal stem cells in keratoconjunctivitis sicca in a canine model. Biomed Res Int, 2015, 2-4.
  • Westhauser F, Karadjian M, Essers C, et al (2019): Osteogenic differentiation of mesenchymal stem cells is enhanced in a 45S5-supplemented β-TCP composite scaffold: an in-vitro comparison of Vitoss and Vitoss BA. PloS One, 14, 1-18.
  • Wilson A, Chee M, Butler P, et al (2019): Isolation and characterisation of human adipose-derived stem cells. Methods Mol Biol, 2019, 3-13.
  • Xiaoming L, Haifeng L, Niu X, et al (2011): Osteogenic differentiation of human adipose‐derived stem cells induced by osteoinductive calcium phosphate ceramics. J Biomed Mater Res B Appl Biomater, 1, 10-19.
  • Zuk PA, Zhu M, Mizuno H, et al (2001): Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng, 7, 211-228.
There are 53 citations in total.

Details

Primary Language English
Subjects Veterinary Histology and Embryology
Journal Section Research Article
Authors

Özge Özgenç 0000-0002-8776-4788

Asuman Özen 0000-0002-9678-0018

Project Number 17L0239015
Publication Date April 1, 2024
Published in Issue Year 2024

Cite

APA Özgenç, Ö., & Özen, A. (2024). Osteogenic differentiation of canine adipose derived mesenchymal stem cells on B‐TCP and B‐TCP/Collagen biomaterials. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 71(2), 125-134. https://doi.org/10.33988/auvfd.1130705
AMA Özgenç Ö, Özen A. Osteogenic differentiation of canine adipose derived mesenchymal stem cells on B‐TCP and B‐TCP/Collagen biomaterials. Ankara Univ Vet Fak Derg. April 2024;71(2):125-134. doi:10.33988/auvfd.1130705
Chicago Özgenç, Özge, and Asuman Özen. “Osteogenic Differentiation of Canine Adipose Derived Mesenchymal Stem Cells on B‐TCP and B‐TCP/Collagen Biomaterials”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 71, no. 2 (April 2024): 125-34. https://doi.org/10.33988/auvfd.1130705.
EndNote Özgenç Ö, Özen A (April 1, 2024) Osteogenic differentiation of canine adipose derived mesenchymal stem cells on B‐TCP and B‐TCP/Collagen biomaterials. Ankara Üniversitesi Veteriner Fakültesi Dergisi 71 2 125–134.
IEEE Ö. Özgenç and A. Özen, “Osteogenic differentiation of canine adipose derived mesenchymal stem cells on B‐TCP and B‐TCP/Collagen biomaterials”, Ankara Univ Vet Fak Derg, vol. 71, no. 2, pp. 125–134, 2024, doi: 10.33988/auvfd.1130705.
ISNAD Özgenç, Özge - Özen, Asuman. “Osteogenic Differentiation of Canine Adipose Derived Mesenchymal Stem Cells on B‐TCP and B‐TCP/Collagen Biomaterials”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 71/2 (April 2024), 125-134. https://doi.org/10.33988/auvfd.1130705.
JAMA Özgenç Ö, Özen A. Osteogenic differentiation of canine adipose derived mesenchymal stem cells on B‐TCP and B‐TCP/Collagen biomaterials. Ankara Univ Vet Fak Derg. 2024;71:125–134.
MLA Özgenç, Özge and Asuman Özen. “Osteogenic Differentiation of Canine Adipose Derived Mesenchymal Stem Cells on B‐TCP and B‐TCP/Collagen Biomaterials”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 71, no. 2, 2024, pp. 125-34, doi:10.33988/auvfd.1130705.
Vancouver Özgenç Ö, Özen A. Osteogenic differentiation of canine adipose derived mesenchymal stem cells on B‐TCP and B‐TCP/Collagen biomaterials. Ankara Univ Vet Fak Derg. 2024;71(2):125-34.

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