Abstract
Adipose-derived stem cells are an attractive alternative as a source of stem cells that can easily be extracted from adipose tissue. Isolation, characterization, and multi-lineage differentiation of adipose-derived stem cells have been described for human and a number of other species. Here we aimed to isolate and characterize camel adipose-derived stromal cell frequency and growth characteristics and assess their adipogenic, osteogenic, and chondrogenic differentiation potential. Samples were obtained from five adult dromedary camels. Fat from abdominal deposits were obtained from each camel and adipose-derived stem cells were isolated by enzymatic digestion as previously reported elsewhere for adipose tissue. Cultures were kept until confluency and subsequently were subjected to differentiation protocols to evaluate adipogenic, osteogenic, and chondrogenic potential. The morphology of resultant camel adipose-derived stem cells appeared to be spindle-shaped fibroblastic morphology, and these cells retained their biological properties during in vitro expansion with no sign of abnormality in karyotype. Under inductive conditions, primary adipose-derived stem cells maintained their lineage differentiation potential into adipogenic, osteogenic, and chondrogenic lineages during subsequent passages. Our observation showed that like human lipoaspirate, camel adipose tissue also contain multi-potent cells and may represent an important stem cell source both for veterinary cell therapy and preclinical studies as well.
Similar content being viewed by others
References
Abu-Tarboush H. M.; Dawood A. A. Cholesterol and fat contents of animal adipose tissues. Food Chem. 46: 89–93; 1993.
Ahmad R.; Wolber W.; Eckardt S.; Koch P.; Schmitt J.; Semechkin R.; Geis C.; Heckmann M.; Brustle O.; Mclaughlin J. K.; Siren A. L.; Muller A. M. Functional neuronal cells generated by human parthenogenetic stem cells. PLoS One 7: e42800; 2012.
Ahmadbeigi N.; Shafiee A.; Seyedjafari E.; Gheisari Y.; Vassei M.; Amanpour S.; Amini S.; Bagherizadeh I.; Soleimani M. Early spontaneous immortalization and loss of plasticity of rabbit bone marrow mesenchymal stem cells. Cell Prolif. 44: 67–74; 2011a.
Ahmadbeigi N.; Soleimani M.; Gheisari Y.; Vasei M.; Amanpour S.; Bagherizadeh I.; Shariati S. A.; Azadmanesh K.; Amini S.; Shafiee A.; Arabkari V.; Nardi N. B. Dormant phase and multinuclear cells: two key phenomena in early culture of murine bone marrow mesenchymal stem cells. Stem Cells Dev. 20: 1337–1347; 2011b.
Al-Nbaheen M.; Vishnubalaji R.; Ali D.; Bouslimi A.; Al-Jassir F.; Megges M.; Prigione A.; Adjaye J.; Kassem M.; Aldahmash A. Human stromal (mesenchymal) stem cells from bone marrow, adipose tissue and skin exhibit differences in molecular phenotype and differentiation potential. Stem Cell Rev.; 2012. doi:10.1007/s12015-012-9365-8.
Al-Sobayil F. A. Circadian rhythm of bone formation biomarkers in serum of dromedary camels. Res. Vet. Sci. 89: 455–459; 2010.
Arrigoni E.; Lopa S.; De Girolamo L.; Stanco D.; Brini A. T. Isolation, characterization and osteogenic differentiation of adipose-derived stem cells: from small to large animal models. Cell Tissue Res. 338: 401–411; 2009.
Baksh D.; Song L.; Tuan R. S. Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J. Cell. Mol. Med. 8: 301–316; 2004.
Braun J.; Hack A.; Weis-Klemm M.; Conrad S.; Treml S.; Kohler K.; Walliser U.; Skutella T.; Aicher W. K. Evaluation of the osteogenic and chondrogenic differentiation capacities of equine adipose tissue-derived mesenchymal stem cells. Am. J. Vet. Res. 71: 1228–1236; 2010.
Caplan A. I. Review: mesenchymal stem cells: cell-based reconstructive therapy in orthopedics. Tissue Eng. 11: 1198–1211; 2005.
Chan W. I.; Hannah R. L.; Dawson M. A.; Pridans C.; Foster D.; Joshi A.; Gottgens B.; Van Deursen J. M.; Huntly B. J. The transcriptional coactivator Cbp regulates self-renewal and differentiation in adult hematopoietic stem cells. Mol. Cell. Biol. 31: 5046–5060; 2011.
Furlani D.; Li W.; Pittermann E.; Klopsch C.; Wang L.; Knopp A.; Jungebluth P.; Thedinga E.; Havenstein C.; Westien I.; Ugurlucan M.; Li R. K.; Ma N.; Steinhoff G. A transformed cell population derived from cultured mesenchymal stem cells has no functional effect after transplantation into the injured heart. Cell Transplant. 18: 319–331; 2009.
Furuya N.; Takenaga M.; Ohta Y.; Tokura Y.; Hamaguchi A.; Sakamaki A.; Kida H.; Handa H.; Nishine H.; Mineshita M.; Miyazawa T. Cell therapy with adipose tissue-derived stem/stromal cells for elastase-induced pulmonary emphysema in rats. Regen. Med. 7: 503–512; 2012.
Gheisari Y.; Azadmanesh K.; Ahmadbeigi N.; Nassiri S. M.; Golestaneh A. F.; Naderi M.; Vasei M.; Arefian E.; Mirab-Samiee S.; Shafiee A.; Soleimani M.; Zeinali S. Genetic modification of mesenchymal stem cells to overexpress CXCR4 and CXCR7 does not improve the homing and therapeutic potentials of these cells in experimental acute kidney injury. Stem Cells Dev.; 2012. doi:10.1089/scd.2011.0588.
Gruber H. E.; Somayaji S.; Riley F.; Hoelscher G. L.; Norton H. J.; Ingram J.; Hanley Jr. E. N. Human adipose-derived mesenchymal stem cells: serial passaging, doubling time and cell senescence. Biotech. Histochem. 87: 303–311; 2012.
Jiang Y.; Jahagirdar B. N.; Reinhardt R. L.; Schwartz R. E.; Keene C. D.; Ortiz-Gonzalez X. R.; Reyes M.; Lenvik T.; Lund T.; Blackstad M.; Du J.; Aldrich S.; Lisberg A.; Low W. C.; Largaespada D. A.; Verfaillie C. M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418: 41–49; 2002.
Kisiel A. H.; McDuffee L. A.; Masaoud E.; Bailey T. R.; Esparza Gonzalez B. P.; Nino-Fong R. Isolation, characterization, and in vitro proliferation of canine mesenchymal stem cells derived from bone marrow, adipose tissue, muscle, and periosteum. Am. J. Vet. Res. 73: 1305–1317; 2012.
Li W. J.; Tuli R.; Huang X.; Laquerriere P.; Tuan R. S. Multilineage differentiation of human mesenchymal stem cells in a three-dimensional nanofibrous scaffold. Biomaterials 26: 5158–5166; 2005.
Marcacci M.; Kon E.; Moukhachev V.; Lavroukov A.; Kutepov S.; Quarto R.; Mastrogiacomo M.; Cancedda R. Stem cells associated with macroporous bioceramics for long bone repair: 6- to 7-year outcome of a pilot clinical study. Tissue Eng. 13: 947–955; 2007.
Meligy F. Y.; Shigemura K.; Behnsawy H. M.; Fujisawa M.; Kawabata M.; Shirakawa T. The efficiency of in vitro isolation and myogenic differentiation of MSCs derived from adipose connective tissue, bone marrow, and skeletal muscle tissue. In Vitro Cell. Dev. Biol. Anim. 48: 203–215; 2012.
Minteer D.; Marra K. G.; Rubin J. P. Adipose-derived mesenchymal stem cells: biology and potential applications. Adv. Biochem. Eng. Biotechnol.; 2012. doi:10.1007/10_2012_146.
Miura M.; Miura Y.; Padilla-Nash H. M.; Molinolo A. A.; Fu B.; Patel V.; Seo B. M.; Sonoyama W.; Zheng J. J.; Baker C. C.; Chen W.; Ried T.; Shi S. Accumulated chromosomal instability in murine bone marrow mesenchymal stem cells leads to malignant transformation. Stem Cells 24: 1095–1103; 2006.
Nadri S.; Soleimani M. Isolation murine mesenchymal stem cells by positive selection. In Vitro Cell. Dev. Biol. Anim. 43: 276–282; 2007.
Newman K. D.; Anderson D. E. Fracture management in alpacas and llamas. Vet. Clin. North Am. Food Anim. Pract. 25: 507–522; 2009.
Orbay H.; Tobita M.; Mizuno H. Mesenchymal stem cells isolated from adipose and other tissues: basic biological properties and clinical applications. Stem Cells Int. 2012: 461718; 2012.
Pittenger M. F.; Mackay A. M.; Beck S. C.; Jaiswal R. K.; Douglas R.; Mosca J. D.; Moorman M. A.; Simonetti D. W.; Craig S.; Marshak D. R. Multilineage potential of adult human mesenchymal stem cells. Science 284: 143–147; 1999.
Qu C. Q.; Zhang G. H.; Zhang L. J.; Yang G. S. Osteogenic and adipogenic potential of porcine adipose mesenchymal stem cells. In Vitro Cell. Dev. Biol. Anim. 43: 95–100; 2007.
Razawi S. M.; Oryan A.; Bahrami S.; Mohammadalipour A.; Gowhari M. Prevalence of Cryptosporidium infection in camels (Camelus dromedarius) in a slaughterhouse in Iran. Trop. Biomed. 26: 267–273; 2009.
Requicha J. F.; Viegas C. A.; Albuquerque C. M.; Azevedo J. M.; Reis R. L.; Gomes M. E. Effect of anatomical origin and cell passage number on the stemness and osteogenic differentiation potential of canine adipose-derived stem cells. Stem Cell Rev; 2012. doi:10.1007/s12015-012-9397-0.
Rosland G. V.; Svendsen A.; Torsvik A.; Sobala E.; Mccormack E.; Immervoll H.; Mysliwietz J.; Tonn J. C.; Goldbrunner R.; Lonning P. E.; Bjerkvig R.; Schichor C. Long-term cultures of bone marrow-derived human mesenchymal stem cells frequently undergo spontaneous malignant transformation. Cancer Res. 69: 5331–5339; 2009.
Seyedjafari E.; Soleimani M.; Ghaemi N.; Shabani I. Nanohydroxyapatite-coated electrospun poly(l-lactide) nanofibers enhance osteogenic differentiation of stem cells and induce ectopic bone formation. Biomacromolecules 11: 3118–3125; 2010.
Shafiee A.; Kabiri M.; Ahmadbeigi N.; Yazdani S. O.; Mojtahed M.; Amanpour S.; Soleimani M. Nasal septum-derived multipotent progenitors: a potent source for stem cell-based regenerative medicine. Stem Cells Dev. 20: 2077–2091; 2011a.
Shafiee A.; Seyedjafari E.; Soleimani M.; Ahmadbeigi N.; Dinarvand P.; Ghaemi N. A comparison between osteogenic differentiation of human unrestricted somatic stem cells and mesenchymal stem cells from bone marrow and adipose tissue. Biotechnol. Lett. 33: 1257–1264; 2011b.
Taha M. F.; Hedayati V. Isolation, identification and multipotential differentiation of mouse adipose tissue-derived stem cells. Tissue Cell 42: 211–216; 2010.
Toupadakis C. A.; Wong A.; Genetos D. C.; Cheung W. K.; Borjesson D. L.; Ferraro G. L.; Galuppo L. D.; Leach J. K.; Owens S. D.; Yellowley C. E. Comparison of the osteogenic potential of equine mesenchymal stem cells from bone marrow, adipose tissue, umbilical cord blood, and umbilical cord tissue. Am. J. Vet. Res. 71: 1237–1245; 2010.
Vidal M. A.; Walker N. J.; Napoli E.; Borjesson D. L. Evaluation of senescence in mesenchymal stem cells isolated from equine bone marrow, adipose tissue, and umbilical cord tissue. Stem Cells Dev. 20: 273–283; 2012.
Yoshimura H.; Muneta T.; Nimura A.; Yokoyama A.; Koga H.; Sekiya I. Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res. 327: 449–462; 2007.
Acknowledgments
This work was supported by a grant from the Stem Cell Technology Research Center, Tehran, Iran. The authors like to thank Miss Lida Langroudi for English editing the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Editor: T. Okamoto
Abdollah Mohammadi-Sangcheshmeh and Abbas Shafiee have equally contributed to this publication.
Rights and permissions
About this article
Cite this article
Mohammadi-Sangcheshmeh, A., Shafiee, A., Seyedjafari, E. et al. Isolation, characterization, and mesodermic differentiation of stem cells from adipose tissue of camel (Camelus dromedarius). In Vitro Cell.Dev.Biol.-Animal 49, 147–154 (2013). https://doi.org/10.1007/s11626-012-9578-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11626-012-9578-9