Development of a perfusion bioreactor for culturing hematopoietic stem cells


Principal Investigator :  Asok Mukhopadhyay

Project Associates/Assistants
T Madhusudhan (till Jan 2004)

Ph D Students
Satish Khurana (since Jan 2004)

Hematopoietic stem cell (HSC) transplantation can provide cure to a variety of malignant and non-malignant hematological diseases. Recently, it has also been observed that bone marrow stem cells are multipotent in nature, that transdifferentiate into various cell types. Inspite of promising new applications, the success of HSC transplantation in different clinical setting largely depends on its availability. Getting sufficient numbers and acceptable quality of progenitor stem cells in right time is difficult and in some time impossible due to various reasons. HSC transplantation would be greatly facilitated by ex vivo expansion of a small number of cells from bone marrow, or peripheral blood, or a cord blood sample. At present, no suitable system is available for ex vivo expansion of stem cells. Thus, the main theme of the project is to develop a prototype bioreactor for culturing adult stem cells. The project aims at development of a bioreactor and its operation for cultivation of hematopoietic stem cells, mimicking bone marrow microenvironment. The objectives of the project are (i) development of a biocompatible three-dimensional (3-D) matrix from natural and/or synthetic polymers and ex vivo expansion of HSC, (ii) study on grafting and transdifferential potential of HSC in bone marrow and in other organ, (iii) molecular control for self-renewal of HSCs, and (iv) development of a prototype bioreactor and its operation for expansion of progenitor stem cells.

Hematopoietic stem cell transplantation is generally carried out after irradiation or treatment with cytotoxic drugs in the notion that host bone marrow ‘niches’ become available to the donor cells for engraftment. How bone marrow stromal cells respond to the radiation, which ultimately modulate grafting of donor cells is poorly understood. We examined homing and marrow retention of PKH-26 labeled donor cells in age matched C57BL/6J mice conditioned at different doses of radiation. When injected donor cells into mice that received lethal radiation of 900 cGy, the percent homing was highest (15.8 ±1.5%) as compared to the lower doses (450 and 200 cGy) of radiation. Despite highest homing of donor cells in these mice, about 70% (p < 0.005) homed cells were detached from the marrow within 72 h of transplantation. In contrast, 2- to 2.5-fold (p < 0.03) multiplication of homed PKH-26+Sca-1+ cells was observed in sub-lethally irradiated mice. The poor retention of homed cells in lethally irradiated mice was believed to be due to the damage of marrow stromal cells that ultimately support the graft. In order to investigate that, the population of non-hematopoietic (stoma) and VCAM-1 positive cells (CD45-CD106+) in bone marrow at different doses of radiation was determined. It was revealed that in lethally irradiated (900 cGy) mice, more than 80% stromal cells were depleted within 72 h of radiation, implicating radiation-induced degeneration of stroma as one of the factors for such poor retention of donor cells. Another important observation made in this study was that the grafted cells confer protection to the endogenous marrow cells from the radiation-induced damage. In order to study whether such observation was transplant dose-dependent, two different dose ranges (5-8 and 12-15 x 106) of cells labeled with PKH-26 dye were injected in sub-lethally irradiated (450 cGy) mice. It was found that in control mice (without grafting) the bone marrow cellularity was declined from 279.2 ± 8.9 x 106 to 106.5 ± 11.7 x 106 within 24 h of radiation. However, following transplantation at two doses of cells, the bone marrow cellularity was increased by 33 and 41%, respectively as compared to the control. The colony forming assay confirmed that in irradiated host the myeloid colony was partially restored by the transplanted cells in dose dependent manner.

In vivo grafting study for 28 days experiment demonstrated that the expression of three integrin adhesion molecules (VLA-4/5/6) in the bone marrow grafted cells were up-regulated in time dependent manner. This probably justifies the physiological requirement of VLA-4/5/6 molecules in the long-term retention of primitive cells in bone marrow. Earlier, it was shown by different groups of investigators that VLA-4/5 adhesion molecules are important for grafting of donor cells to the marrow. Therefore, ex vivo expansion of murine stem cells was carried out in the notion that the expression of these adhesion molecules will be restored, if not up-regulated. It was found that the expression of VLA-5 and –6 were increased up to 2 to 3-fold, where as that of o1-integrin (CD29) was restored in 5 day culture in presence of cytokines. Contrary to that, the expression of VLA-4 in the cultured cells was decreased. How the expression of o4-integrin in the cultured cells modulated is the subject of present investigated.

Evidence from recent reports suggest that hematopoietic stem cells may have unexpected developmental plasticity, which means that these cells differentiate in to cells of other tissues under suitable culture conditions. It is crucial to comprehend the underlying mechanisms governing the cell fate decisions, so that the clinical benefits of HSCs in tissue regeneration and gene therapy can be maximized. To determine such mechanism PKH-26 labeled cells derived from bone marrow were transplanted into age matched mice. It was revealed that about 60 ± 5.4% donor cells homed to the liver and stayed there at least for one month without multiplication. By cell cycle analysis, it was confirmed that about 92% of the grafted cells were maintained in the G0-G1 phase. The homed cells were uniformly distributed in the liver, as confirmed by histological analysis of the cryosection. The phenotypes of the homed cells were gradually changed, as the characteristic hematopoietic cell markers like CD45.1 and CD11b were dropped from 94 % to 20% and 40% to 20%, respectively. Colony forming cell assay also indicated that the functional property of the bone marrow specific cells was modulated in the liver. In comparison, the cells grafted in the bone marrow multiplied and maintained typical properties of the cells, indicating that the cellular microenvironment is influential in determining the fate of the cell. Though it is clear from the present study that the phenotypes of hematopoietic cells grafted in the liver is changed, but it is yet to be known whether these cells acquire hepatocyte specific phenotype and/or hepatocyte specific function.

Publications

Original peer-reviewed articles

1.     *Mashusadan T, Richhariya A, Mazumder S and Mukhopadhyay A (2003) An in vitro model for grafting of hematopoietic stem cells predicts bone marrow reconstitution of a myeloablative mice. J Hematother Stem Cell Res 12:243-252 (*in press last year, since published).

2.     †Takada Y, Mukhopadhyay A, Kundu GC, Mahabeleshwar GH, Singh S and Aggarwal BB (2003) Hydrogen peroxide activates NF-kB through tyrosine phosphorylation of IkBa and serine phosphorylation of P65: evidence for the involvement of IkB kinase and Syk protein tyrosine kinase. J Biol Chem 278:24233-24241 (†on deputation/work done elsewhere).

3.     Raju GMK, Guha S, Mukhopadhyay A, Kumar L, Kale VP, Mittal S, Deka D, Mohanty S and Kochupillai V (2003) Colony-stimulating activity of fetal liver cells:synergistic role of stem cell factor in bone marrow recovery from aplastic anemia. J Hematother Stem Cell Res 12:491-498.

4.     Mashusadan T, Mazumder S and Mukhopadhyay A (2004) Degeneration of stroma reduces retention of homed cells in bone marrow of lethally irradiated mice. Stem Cells Dev (in press).

Reviews/Proceedings

1.     *Mukhopadhyay A, Madhusudhan T and Kumar R (2003) Hematopoietic stem cells: Clinical requirements and developments in ex vivo culture. Adv Biochem Eng Biotechnol 86:215-253 (*in press last year, since published).