Ali ŞAHİN, Taha KELEŞTEMUR, Bilgehan SOLMAZ, Erkan KAPTANOĞLU, Ertuğrul KILIÇ

Evidence that osteogenic and neurogenic differentiation capability of epidural adipose tissue-derived stem cells was more pronounced than in subcutaneous cells

Background/aim: The management of dura-related complications, such as the repairment of dural tears and reconstruction of large dural defects, remain the most challenging subjects of neurosurgery. Numerous surgical techniques and synthetic or autologous adjuvant materials have emerged as an adjunct to primary dural closure, which may result in further complications or side effects. Therefore, the subcutaneous autologous free adipose tissue graft has been recommended for the protection of the central nervous system and repairment of the meninges. In addition, human adipose tissue is also a source of multipotent stem cells. However, epidural adipose tissue seems more promising than subcutaneous because of the close location and intercellular communication with the spinal cord. Herein, it was aimed to define differentiation capability of both subcutaneous and epidural adipose tissue-derived stem cells (ASCs). Materials and methods: Human subcutaneous and epidural adipose tissue specimens were harvested from the primary incisional site and the lumbar epidural space during lumbar spinal surgery, and ASCs were isolated. Results: The results indicated that both types of ASCs expressed the cell surface markers, which are commonly expressed stem cells; however, epidural ASCs showed lower expression of CD90 than the subcutaneous ASCs. Moreover, it was demonstrated that the osteogenic and neurogenic differentiation capability of epidural adipose tissue-derived ASCs was more pronounced than that of the subcutaneous ASCs. Conclusion: Consequently, the impact of characterization of epidural ASCs will allow for a new understanding for dural as well as central nervous system healing and recovery after an injury.

PDF

___

1. Cammisa FP, Girardi FP, Sangani PK, Parvataneni HK, Cadag S et al. Incidental durotomy in spine surgery. Spine 2000; 25 (20): 2663-2667. Doi 10.1097/00007632-200010150-00019
2. Shaffrey CI, Spotnitz WD, Shaffrey ME, Jane JA. Neurosurgical applications of fibrin glue: augmentation of dural closure in 134 patients. Neurosurgery 1990; 26 (2): 207-210
3. Black P. Cerebrospinal fluid leaks following spinal surgery: use of fat grafts for prevention and repair. Technical note. Journal of Neurosurgery 2002; 96 (2 Suppl): 250-252
4. Mayfield FH. Autologous fat transplants for the protection and repair of the spinal dura. Clinical Neurosurgery 1980; 27: 349- 361
5. Costantino PD, Wolpoe ME, Govindaraj S, Chaplin JM, Sen C et al. Human dural replacement with acellular dermis: Clinical results and a review of the literature. Head and Neck-Journal for the Sciences and Specialties of the Head and Neck 2000; 22 (8): 765-771. Doi 10.1002/1097-0347
6. Wong VW, Levi B, Rajadas J, Longaker MT, Gurtner GC. Stem cell niches for skin regeneration. International Journal of Biomaterials 2012; 2012: 926059. doi 10.1155/2012/926059
7. Lu L, Finegold MJ, Johnson RL. Hippo pathway coactivators Yap and Taz are required to coordinate mammalian liver regeneration. Experimental and Molecular Medicine 2018; 50ARTN e42310.1038/emm.2017.205
8. Wong VW, Levi B, Rajadas J, Longaker MT, Gurtner GC. Stem cell niches for skin regeneration. International Journal of Biomaterials 2012; 2012: 926059. doi 10.1155/2012/926059
9. Decimo I, Bifari F, Rodriguez FJ, Malpeli G, Dolci S et al. Nestin- and Doublecortin-Positive Cells Reside in Adult Spinal Cord Meninges and Participate in Injury-Induced Parenchymal Reaction. Stem Cells 2011; 29 (12): 2062-2076. doi 10.1002/stem.766
10. Tardieu GG, Fisahn C, Loukas M, Moisi M, Chapman J et al. The Epidural Ligaments (of Hofmann): A Comprehensive Review of the Literature. Cureus 2016; 8 (9) UNSP e77910.7759/ cureus.779
11. Beaujeux R, WolframGabel R, Kehrli P, Fabre M, Dietemann JL et al. Posterior lumbar epidural fat as a functional structure? Histologic specificities. Spine 1997; 22 (11): 1264-1268. Doi 10.1097/00007632-199706010-00021
12. Reina MA, Franco CD, Lopez A, De Andres JA, van Zundert A. Clinical implications of epidural fat in the spinal canal. A scanning electron microscopic study. Acta Anaesthesiologica Belgica 2009; 60 (1): 7-17
13. Gagliardi C, Bunnell BA. Isolation and culture of rhesus adipose-derived stem cells. Methods in Molecular Biology 2011; 702: 3-16. doi 10.1007/978-1-61737-960-4_1
14. Bourin P, Bunnell BA, Casteilla L, Dominici M, Katz AJ et al. Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/ stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy 2013; 15 (6): 641-648. doi 10.1016/j.jcyt.2013.02.006
15. Gagliardi C, Bunnell BA. Isolation and culture of rhesus adipose-derived stem cells. Methods in Molecular Biology 2011; 702:3-16. doi 10.1007/978-1-61737-960-4_1
16. Berry DC, Stenesen D, Zeve D, Graff JM. The developmental origins of adipose tissue. Development 2013; 140 (19): 3939- 3949. doi 10.1242/dev.080549
17. Martinez-Santibanez G, Cho KW, Lumeng CN. Imaging White Adipose Tissue with Confocal Microscopy. Methods of Adipose Tissue Biology, Pt A 2014; 537: 17-30. doi 10.1016/ B978-0-12-411619-1.00002-1
18. Tchkonia T, Thomou T, Zhu Y, Karagiannides I, Pothoulakis C et al. Mechanisms and Metabolic Implications of Regional Differences among Fat Depots. Cell Metabolism 2013; 17 (5): 644-656. doi 10.1016/j.cmet.2013.03.008
19. Reina MA, Franco CD, Lopez A, De Andres JA, van Zundert A. Clinical implications of epidural fat in the spinal canal. A scanning electron microscopic study. Acta Anaesthesiologica Belgica 2009; 60 (1): 7-17
20. Thomou T, Tchkonia, T., and Kirkland, J.L. Cellular and molecular basis of functional differences among fat depots. In: G. TALaJG (editor), Adipose Tissue in Health and Disease. Weinheim, Germany: Wiley; 2010.
21. Kruglikov IL, Scherer PE. Dermal Adipocytes: From Irrelevance to Metabolic Targets? Trends in Endocrinology & Metabolism 2016; 27 (1): 1-10 10.1016/j.tem.2015.11.002
22. Zwick RK, Guerrero-Juarez CF, Horsley V, Plikus MV. Anatomical, Physiological, and Functional Diversity of Adipose Tissue. Cell Metabolism 2018; 27 (1): 68-83. doi 10.1016/j.cmet.2017.12.002
23. Sanchez-Gurmaches J, Guertin DA. Adipocyte lineages: Tracing back the origins of fat. Biochimica Et Biophysica Acta-Molecular Basis of Disease 2014; 1842 (3): 340-351. doi 10.1016/j.bbadis.2013.05.027
24. Raposio E, Guida C, Baldelli I, Benvenuto F, Curto M et al. Characterization and induction of human pre-adipocytes. Toxicology in Vitro 2007; 21 (2):330-334. doi 10.1016/j. tiv.2006.09.022
25. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI et al. Human adipose tissue is a source of multipotent stem cells. Molecular Biology of the Cell 2002; 13 (12): 4279-4295. doi 10.1091/mbc.E02-02-0105
26. Gnanasegaran N, Govindasamy V, Musa S, Kasim NH. Different isolation methods alter the gene expression profiling of adipose derived stem cells. International Journal of Medical Sciences 2014; 11 (4): 391-403. doi 10.7150/ijms.7697
27. Baer PC, Geiger H. Adipose-Derived Mesenchymal Stromal/ Stem Cells: Tissue Localization, Characterization, and Heterogeneity. Stem Cells International 2012Unsp 812693 10.1155/2012/812693
28. Williams AF, Gagnon J. Neuronal cell Thy-1 glycoprotein: homology with immunoglobulin. Science 1982; 216 (4547): 696-703
29. Chen XD, Qian HY, Neff L, Satomura K, Horowitz MC. Thy1 antigen expression by cells in the osteoblast lineage. Journal of Bone and Mineral Research 1999; 14 (3): 362-375 10.1359/ jbmr.1999.14.3.362
30. Moraes DA, Sibov TT, Pavon LF, Alvim PQ, Bonadio RS et al. A reduction in CD90 (THY-1) expression results in increased differentiation of mesenchymal stromal cells. Journal of Stem Cell Research & Therapy 2016; 7 (1): 97 10.1186/s13287-016- 0359-3
31. Wiesmann A, Buhring HJ, Mentrup C, Wiesmann HP. Decreased CD90 expression in human mesenchymal stem cells by applying mechanical stimulation. Head & Face Medicine 2006; 2:8. doi 10.1186/1746-160X-2-8
32. Frese L, Dijkman PE, Hoerstrup SP. Adipose Tissue-Derived Stem Cells in Regenerative Medicine. Transfusion Medicine and Hemotherapy 2016; 43 (4): 268-274. doi 10.1159/000448180
33. Cardozo AJ, Gomez DE, Argibay PF. Neurogenic differentiation of human adipose-derived stem cells: Relevance of different signaling molecules, transcription factors, and key marker genes. Gene 2012; 511 (2): 427-436. doi 10.1016/j. gene.2012.09.038
34. Andreazzoli M, Angeloni D, Broccoli V, Demontis GC. Microgravity, Stem Cells, and Embryonic Development: Challenges and Opportunities for 3D Tissue Generation. Frontiers in Astronomy and Space Sciences 2017; 4UNSP 210.3389/fspas.2017.00002
35. Kang SK, Putnam LA, Ylostalo J, Popescu IR, Dufour J et al. Neurogenesis of Rhesus adipose stromal cells. Journal of Cell Science 2004; 117 (18): 4289-4299. doi 10.1242/jcs.01264
36. Ashjian PH, Elbarbary AS, Edmonds B, DeUgarte D, Zhu M et al. In vitro differentiation of human processed lipoaspirate cells into early neural progenitors. Plastic and Reconstructive Surgery 2003; 111 (6): 1922-1931. doi 10.1097/01. Prs.0000055043.62589.05
37. Jang S, Cho HH, Cho YB, Park JS, Jeong HS. Functional neural differentiation of human adipose tissue-derived stem cells using bFGF and forskolin. Bmc Cell Biology 2010; 11Artn 25. doi 10.1186/1471-2121-11-25
38. Feng JF, Mantesso A, De Bari C, Nishiyama A, Sharpe PT. Dual origin of mesenchymal stem cells contributing to organ growth and repair. Proceedings of the National Academy of Sciences of the United States of America 2011;108 (16): 6503-6508. doi 10.1073/pnas.1015449108
39. Majka SM, Fox KE, Psilas JC, Helm KM, Childs CR et al. De novo generation of white adipocytes from the myeloid lineage via mesenchymal intermediates is age, adipose depot, and gender specific. Proceedings of the National Academy of Sciences of the United States of America 2010; 107 (33): 14781- 14786. doi 10.1073/pnas.1003512107
40. Slukvin II, Vodyanik M. Endothelial origin of mesenchymal stem cells. Cell Cycle 2011; 10 (9): 1370-1373. doi 10.4161/ cc.10.9.15345
41. Billon N, Iannarelli P, Monteiro MC, Glavieux-Pardanaud C, Richardson WD et al. The generation of adipocytes by the neural crest. Development 2007; 134 (12): 2283-2292. doi 10.1242/dev.002642
42. Lemos DR, Paylor B, Chang C, Sampaio A, Underhill TM et al. Functionally Convergent White Adipogenic Progenitors of Different Lineages Participate in a Diffused System Supporting Tissue Regeneration. Stem Cells 2012; 30 (6): 1152-1162. doi 10.1002/stem.1082
43. Sowa Y, Imura T, Numajiri T, Takeda K, Mabuchi Y et al. Adipose Stromal Cells Contain Phenotypically Distinct Adipogenic Progenitors Derived from Neural Crest. PLoS One 2013; 8 (12)ARTN e8420610.1371/journal.pone.0084206