International Journal of Current Research and Review
ISSN: 2231-2196 (Print)ISSN: 0975-5241 (Online)
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IJCRR - 2(9), September, 2010

Pages: 13-22

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CHARACTERIZATION OF CYTOTHERAPEUTIC POTENTIAL OF SUBPOPULATION VERSUS
STEMCELLS FROM BONE MARROW

Author: Dhanasekaran Marappagoundar, Indumathi Somasundaram, Sowndarya sampath, Baskaran Mayakesavan, Rajkumar Sankaran, Sudarsanam Dorairaj

Category: Healthcare

Abstract:Research on adult stem cells has been a great deal of excitement. The candidate stem
cells present in the adult tissues are the hematopoietic and mesenchymal stem cells.
However, there exist other heterogenous cell such as side population (SP) and
endothelial progenitors (EP) that has the properties of repair and regeneration. Much
work pertaining to these subpopulations is at its infancy and more research in clinical
practice is of utmost important. Thus, the objective of this work is to find out whether
subpopulations exist in bone marrow in higher percentage and play a vital role in tissue
repair and regeneration. To test this hypothesis, we characterized stem cell populations
versus subpopulations including EP cells and SP cells from Bone Marrow samples (n =
5). Surprisingly, we found that the mean of Endoglin CD105+ CD34-, CD105+ CD90 -
for EP cells was found to be 41.68% and 35.88% respectively. The mean of ABCG2+
and CD117+ SP cells was found to be 3.58% and 4.34%. These results confirm the
hypothesis and emphasize on the fact that migration at the site of injury in vivo and
recovery not only depends on the candidate stem cells but also require the heterogenous
subpopulation cells to regulate the candidate stem cells because of the wide plasticity
and common precursor called hemangioblast. Thus, we conclude that the
subpopulations of especially ABCG2 + and CD105+ found to be a potent source of
repair mechanism and hence need to be more focused on research.

Keywords: Hematopoietic Stem cells, Mesenchymal stem cells, ABCG2+ Side population cells, Endoglin, Fluorescent Activated Cell Sorter.

Full Text:

INTRODUCTION

The therapy through cell transplant has been developed based on the adult multipotent stem cell that is becoming, consequently, an important scientific subject.1 It has already been proved that most promising stem cell source in clinical practice is represented by bone marrow with more focus on candidate stem cells especially HSC and MSC.1 However, recent development in stem cell biology has demonstrated the presence of sub population cells,

especially side population (SP) cells and endothelial progenitor (EP) cells along with stem cells which is said to possess the properties of repair and regeneration.2, 3, 4 Side population cells were first identified as a subpopulation of very primitive CD 34- negative hematopoietic stem cells (HSCs) with long term hematopoietic repopulation activity, which was characterized by their capacity to efflux Hoechst 33342 and was acquired by the expression of the ATP-binding cassette transporters such as Bcrp 1 / ABCG2.3, 5 This has been identified to produce a characteristic SP profile on basis of FACS analysis, regardless of tissue origin. Isolation of SP cells by the Hodye and FACS technique has been reported in Muscular tissue6 , Liver7 , Lung8 , Skin9 , uterus10, Testis11 , Cornea12 and Bone marrow13 . Apart from the side population cells, important subpopulation cells found to possess repair mechanism and neovascularization is Endothelial Progenitor cells that circulate in adult tissues.14 According to the initial discoveries, EPC are defined as cell positive for both hematopoietic stem cell marker such as CD34+ and an endothelial marker protein VEGFR2 as this endothelial progenitor cells have consequently been considered to device from a common precursors putatively termed a hemangioblast.15 Asahara and colleagues published that purified CD 34+ hematopoietic progenitor cells from adults can differentiate ex vivo to an endothelial phenotype.16 Much work does not exist on cell surface characterization and importance of EP cells and SP cell in Bone Marrow. Moreover, focus on homogenous candidate stem cells by sorting of CD 34+ HSC by FACS17, lineage depletion by MACS18, 19 and expansion of MSC in culture20 gained importance in cell therapy.

Hence, we speculated that heterogenous subpopulation cells play a vital role in repair mechanism and faster engraftment by regulating stem cell population of Bone marrow and not homogenous stem cells like HSC and MSC alone possess cytotherapeutic potential. To test this speculated hypothesis we analyzed the percentage of subpopulation cells especially CD 105+ Endothelial cells and CD117+ABCG2+ side population from Bone marrow ( n= 5) mononuclear cells in comparison with CD34+ HSC and CD90+ MSC using FACS. The results demonstrated in this study provide evidence for our speculation. However, further research is required to address our speculations to make bone marrow mononuclear cell therapy successful.

MATERIALS AND METHODS

Reagents used: The following antibodies conjugated with corresponding flurochromes (CD34-PE; Cat No: 348057, CD117- PE-Cy7; Cat No: 339195, CD-90-PERCP-Cy5; Cat No: 555597, Cell viability dye 7-AAD; Cat No: 555816) were purchased from BD Biosciences, (http://www.bd.com/). CD105-APC; Cat No: 17-1057 and ABCG2-PE; Cat No: 12-8888 were purchased from eBioscience, (www.ebioscience.com).

Ficoll Paque Plus; Cat No: 07917 were purchased from stem cell technologies, (www.stemcell.com). Phosphate Buffer Saline (PBS); Cat No: TL1032 were purchased from Himedia.

Bone marrow collection:

Human Bone marrow samples were obtained from the iliac crest of 5 patients with spinal cord injury – paraplegia who was aged between 25 – 40 years and who had applied for a stem cell transplantation procedure after the approval of Institutional ethics committee. Formal written consent from the donors was obtained before collection. About 10 ml of BM aspirate were collected in a syringe containing heparin to prevent coagulation.

Isolation procedure:

The bone marrow sample was diluted 1:2 with 1 X Phosphate Buffer Saline (PBS) and carefully layered on to Ficoll Paque (1.077g/mL) slowly along the sides of the tube at 45� angle to isolate Bone marrow Mononuclear cells (MNCs). The MNCs were isolated by density gradient centrifugation (400g, 30 minutes, room temperature). Further, cells were washed twice with PBS (450g, 10 minutes, room temperature) to remove residual Ficoll and other contaminants. The pellet was resuspended with RBC lysis buffer solution for 10 minutes and immediately treated with 0.9% cold NaCl to stop the lysis reaction and centrifuged (300g, 5 minutes, 4º C). Cell viability was determined using the Trypan blue dye exclusion method using hemocytometry. The mononuclear cells were characterized for various hematopoietic, mesenchymal and subpopulation cells with its surface markers using flowcytometry.

Flowcytometric protocol for

characterization:

Flow cytometry was performed on a Becton, Dickinson FACS Aria (http://www.bd.com/) using a 488-nm argon-ion LASER and 632nm red LASER for excitation; fluorescence emission was collected using its corresponding detectors. 1X106 cells were stained with appropriate amount of conjugated antibodies in each of 12X75 mm falcon polystyrene FACS tube, BD Bioscience; Cat No: 352054. The quantity of each antibody conjugated with fluorochromes added to the cells in each tube were 20μl of CD34-PE, 5μl of CD90- PER CP CY5, 20μl of CD 105-APC, 5μl of CD117-PE CY7, 20μl of ABCG2-PE, 20μl of 7- AAD (BD Via probe), respectively. All tubes were incubated for 20 minutes in dark. After incubation, cells were washed in phosphate buffer saline to remove the unbound antibodies. The pellet was further resuspended to 500μl. Data analysis and acquisition was then performed using DIVA Software, Becton Dickinson. Flow cytometer instruments were set using unstained cells. Cells were gated by forward versus side scatter to eliminate debris. The number of cells staining positive for a given marker was determined by the percentage of cells present within a gate established. A minimum of 10 000 events was characterized and recorde

DISCUSSION

It has already been proved that Bone marrow is the promising source of stem cell therapy with presence of HSC and MSC2 . The Efficiency of the processed mononuclear cell from Bone marrow is of utmost importance before cellular characterization or cellular transplant. Thus in our study to confirm whether processed Bone marrow MNC (n=5) are devoid of contaminants and is highly efficient for further research and therapy, we performed a differential count analysis before and after MNC processing (Figure 1, Table 1). Though granulocytes live only ~10hrs in circulation, there exist many complications of granulocyte interface with MNC. It might even disrupt the stem cells from further engraftment. Hence, we emphasize on the fact that this must be an essential step for any researcher working on MNC isolation for cell transplant or research to yield better and efficient result. Recently, focus on homogenous candidate stem cells by sorting of CD 34+ HSC by FACS17, 18 , lineage depletion by MACS19 and expansion of MSC in culture20, 21 has gained importance in research for cellular transplant than mononuclear cell (MNC) therapy. However, homogenous HSC population or MSC from Bone marrow has a vast disadvantage. MSC decreases as age increases22 and phenotypic variations exist in each MSC population from various sources.23 Likewise, pure HSC population exhibit less percentage and are not plastic as well compared to heterogenous MNC.24 Moreover, by isolating or sorting pure HSC/MSC population for transplant, faster engraftment and recovery might not be fully satisfied. Existing evidence suggests that EP cells of CD34+CD133+Flk+ possess efficient repair mechanism of neovascularization in Ischemia.4, 14, 15 Much work on EP cell plasticity is not widely studied and CD 105+ Endoglin which is said to be putative EP cell population is also not much focused in research. Likewise, Presence of side population cells has been shown in many adult tissues and the SP phenotype might be represented as a common molecular regulatory feature for a wide variety of stem cells.5 However, importance of CD117+ABCG2+ SP cell research exists much only on tumor cell not in bone marrow cells.25, 26 Thus we speculated that Bone marrow, being heterogenous, not only contain HSC/MSC but also subpopulation especially EP & SP cells which serves to be an effective repair mechanism. To confirm our speculated hypothesis, in our experiment, we analyzed the percentage of subpopulation cells especially CD 105+ EP cells and CD117+ABCG2+ SP cells from Bone marrow ( n= 5) mononuclear cells in comparison with CD34+ HSC and CD90+ MSC using FACS. The results demonstrated in this study provide evidence for our speculation. We found that Bone marrow MNC contain more percentage of CD 105+ EP cells compared to CD105+ cells obtained from other research works of Takayuki Asahara et al16. We also found that CD105+ EP cell percentage is found to be much higher compared to CD34+CD133+ EP cells obtained from Carmen Urbich et al, 2006 and Mihali Hristov et al, 20034, 14. Similarly, several researchers have demonstrated that the percentage of SP cells from bone marrow ranges between 0.01- 3.0 %.3,5 In contrast to the existing data, the percentage of ABCG2+CD117+ SP cells in our results from all 5 samples was found to be much higher (Figure 3& Bar diagram 2). Moreover, the percentage of CD105+ and CD117+ABCG2+ from bone marrow is found to be higher than the percentage obtained from stromal vascular fraction of subcutaneous and omentum fat tissue from our previous research work.27 This confirms that the Subpopulation cells are exhibited in higher percentage in bone marrow compared to adipose tissue. Finally it is evident from our research work that the migration at the site of injury and recovery in vivo not only depends on the candidate stem cells ( HSC and MSC) but also require the heterogenous subpopulation (EP and SP) cells to regulate the candidate stem cells. Thus, we emphasize that Bone marrow mononuclear cells are the best source of clinical transplants unlike homogenous HSC and MSC population because of the vast heterogeneity and plasticity. However, further research on these subpopulation cells will bring this work closer to clinical applications.

References:

1. Ana maria cristina serban, Gabriela Tanasie, Daciana Nistor. ?Stem cell types in Bone marrow?. TMJ 2008; 58: 3-4.

2. Challen GA, Little MH. Aside order of stem cells: The SP Phenotype. Stem cells 2006; 24: 3-12

3. Margaret A. Goodell, Shannon McKinney-freeman and Fernando D. Camargo Isolation and characterization of side population cells. Mol bio 1996; 290.

4. Carmen Urbich and Stefanie Dimmeler. Endothelial progenitor cells: Characterization and role in vascular biology. Circ.Res 2006; 95: 343-353.

5. Guo Y, Follo M, Geiger K, Lubbert M, Engelhard M. Side population cells from different precursor compartments. Stem cell Res 2003; 12: 71-82.

6. Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK, Goodell MA. Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest. 2001; 107:1395–1402.

7. Shimano K, Satake M, Okaya A, Kitanaka J, Kitanaka N, et al. Hepatic oval cells have the side population phenotype defined by expression of ATP-binding cassette transporter ABCG2/BCRP1. Am J Pathol 2003; 163:3–9

8. Majka SM, Beutz MA, Hagen M, Izzo AA, Voelkel N, Helm KM. Identification of novel resident pulmonary stem cells: form and function of the lung side population. Stem Cells 2005; 23:1073–1081.

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10. Ono M, Maruyama T, Masuda H, Kajitani T, Nagashima T, Arase T et al. Side population in human uterine myometrium displays phenotypic and functional characteristics of myometrial stem cells. Proc Natl Acad Sci USA 2007; 104:18700–5.

11. Lassalle B, Bastos H, Louis JP, Riou L, Testart J, Dutrillaux B, Fouchet P, Allemand I. 'Side Population' cells in adult mouse testis express Bcrp1 gene and are enriched in spermatogonia and germinal stem cells. Development 2004; 131:479–87.

12. Du Y, Funderburgh ML, Mann MM, SundarRaj N, Funderburgh JL. Multipotent stem cells in human corneal stroma. Stem Cells. 2005; 23:1266–1275.

13. Jihyun Yoon, Seung- Cheol Choi, Chi-yeon park, Ji-Hyun choi, Yangin Kim, Wan-Joo Shim and Do-sun Lim. Bone marrow derived side population cells are capable of functional cardiomyogenic differentiation. Mol. Cells 2008; 25,2:216-223.

14. Mihail Hristov, Wolfgang Erl and Peter C. Weber), Endothelial progenitor cells: Mobilization, Differentiation, and Homing. Arterioscler Thromb Vasc Biol 2006; 23:1185-1189.

15. Taka yuki Asahara, Haruchika Masuda, Tomono Takahashi, Christoph Kalka, Christopher Pastore, Marcy Silver, Marianne Kearne, Meredith Magner, Jeffrey M. Isner. Bone marrow origin of Endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological Neovascularization. Circ. Res 1999; 85: 221-228.

16. Asahara T, Murohara T, Sullivan A, Silver M, Van der zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997; 275:964-967.

17. Loken MR. Immunoflourescence techniques in flowcytometry and sorting. Weiley 1990; 341-353.

18. Dhahlke MH, Lauto OS, Jager MD, et al.. In vivo depletion of hematopoietic stem cells in the rat by an anti- CD45 (RTT) antibody. Blood 2002; 35: 66-72

19. Forraz N, Pettengell R, McGuckin CP. Characterization of a lineage negative stem progenitor cell population optimized for ex vivo expansion and enriched for LTCIC. Stem cells 2004; 22(1): 100 - 8.

20. Granthos , Zannettino AC. A method to isolate and purify bone marrow stromal stem cells. Methods Mol Bio. 2008;449:45-57

21. Le Blanc K. Mesenchymal stromal cells: tissue repair and immune modulation. Cytotherapy 2006; 8:559–561.

22. Mueller SM, Glowacki J. Agerelated decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional 22 International Journal of Current Research and Review www.ijcrr.com Vol. 02 issue 9 Sep 2010 collagen sponges. J Cell Biochem 2001; 82:583–590.

23. Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W, Ho AD. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005; 33:1402–1416.

24. Laurent roybon, zhi ma, fredrik asztely, et al. Failure of Transdifferentiation of Adult Hematopoietic Stem Cells into Neurons. STEMCELLS 2006; 24:1594–1604

25. C.Hirschmann-jax, Foster. A.E, Wulf.G.G, Nuchtern.J.G, Jax.T.W, Gobel.U, Goodell.M.A., Brenner.M.K. A distinct side population of cells with high drug efflux capacity in human tumor cells. 2004.

26. Colleen Wu, Qingxia Wei, Velani Utemo et al. Side population cells isolated from mesenchymal neoplasms have tumor initiating potential. Cancer research 2007; 67: 8216.

27. Dhanasekaran Marappagoundar, Indumathi Somasundaram et al. Characterization of Hematopoietic stem cells, mesenchymal stem cells and side population cells from adipose tissue. International Journal of Biology 2010; 2(1): 71-78.

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A Study by Juna Byun et al. entitled "Study on Difference in Coronavirus-19 Related Anxiety between Face-to-face and Non-face-to-face Classes among University Students in South Korea" is awarded Best Article for Vol 12 issue 16
A Study by Sudha Ramachandra & Vinay Chavan entitled "Enhanced-Hybrid-Age Layered Population Structure (E-Hybrid-ALPS): A Genetic Algorithm with Adaptive Crossover for Molecular Docking Studies of Drug Discovery Process" is awarded Best article for Vol 12 issue 15
A Study by Varsha M. Shindhe et al. entitled "A Study on Effect of Smokeless Tobacco on Pulmonary Function Tests in Class IV Workers of USM-KLE (Universiti Sains Malaysia-Karnataka Lingayat Education Society) International Medical Programme, Belagavi" is awarded Best article of Vol 12 issue 14, July 2020
A study by Amruta Choudhary et al. entitled "Family Planning Knowledge, Attitude and Practice Among Women of Reproductive Age from Rural Area of Central India" is awarded Best Article for special issue "Modern Therapeutics Applications"
A study by Raunak Das entitled "Study of Cardiovascular Dysfunctions in Interstitial Lung Diseas epatients by Correlating the Levels of Serum NT PRO BNP and Microalbuminuria (Biomarkers of Cardiovascular Dysfunction) with Echocardiographic, Bronchoscopic and HighResolution Computed Tomography Findings of These ILD Patients" is awarded Best Article of Vol 12 issue 13 
A Study by Kannamani Ramasamy et al. entitled "COVID-19 Situation at Chennai City – Forecasting for the Better Pandemic Management" is awarded best article for  Vol 12 issue 12
A Study by Muhammet Lutfi SELCUK and Fatma entitled "Distinction of Gray and White Matter for Some Histological Staining Methods in New Zealand Rabbit's Brain" is awarded best article for  Vol 12 issue 11
A Study by Anamul Haq et al. entitled "Etiology of Abnormal Uterine Bleeding in Adolescents – Emphasis Upon Polycystic Ovarian Syndrome" is awarded best article for  Vol 12 issue 10
A Study by entitled "Estimation of Reference Interval of Serum Progesterone During Three Trimesters of Normal Pregnancy in a Tertiary Care Hospital of Kolkata" is awarded best article for  Vol 12 issue 09
A Study by Ilona Gracie De Souza & Pavan Kumar G. entitled "Effect of Releasing Myofascial Chain in Patients with Patellofemoral Pain Syndrome - A Randomized Clinical Trial" is awarded best article for  Vol 12 issue 08
A Study by Virendra Atam et. al. entitled "Clinical Profile and Short - Term Mortality Predictors in Acute Stroke with Emphasis on Stress Hyperglycemia and THRIVE Score : An Observational Study" is awarded best article for  Vol 12 issue 07
A Study by K. Krupashree et. al. entitled "Protective Effects of Picrorhizakurroa Against Fumonisin B1 Induced Hepatotoxicity in Mice" is awarded best article for issue Vol 10 issue 20
A study by Mithun K.P. et al "Larvicidal Activity of Crude Solanum Nigrum Leaf and Berries Extract Against Dengue Vector-Aedesaegypti" is awarded Best Article for Vol 10 issue 14 of IJCRR
A study by Asha Menon "Women in Child Care and Early Education: Truly Nontraditional Work" is awarded Best Article for Vol 10 issue 13
A study by Deep J. M. "Prevalence of Molar-Incisor Hypomineralization in 7-13 Years Old Children of Biratnagar, Nepal: A Cross Sectional Study" is awarded Best Article for Vol 10 issue 11 of IJCRR
A review by Chitra et al to analyse relation between Obesity and Type 2 diabetes is awarded 'Best Article' for Vol 10 issue 10 by IJCRR. 
A study by Karanpreet et al "Pregnancy Induced Hypertension: A Study on Its Multisystem Involvement" is given Best Paper Award for Vol 10 issue 09

List of Awardees

A Study by Ese Anibor et al. "Evaluation of Temporomandibular Joint Disorders Among Delta State University Students in Abraka, Nigeria" from Vol 13 issue 16 received Emerging Researcher Award


A Study by Alkhansa Mahmoud et al. entitled "mRNA Expression of Somatostatin Receptors (1-5) in MCF7 and MDA-MB231 Breast Cancer Cells" from Vol 13 issue 06 received Emerging Researcher Award


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International Journal of Current Research and Review (IJCRR) provides platform for researchers to publish and discuss their original research and review work. IJCRR can not be held responsible for views, opinions and written statements of researchers published in this journal

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