Cord Blood Transplantation and Biology

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1 Cord Blood Transplantation and Biology Hal E. Broxmeyer Introduction Three tissue sources of hematopoietic stem and progenitor cells are currently being used for transplantation purposes.1 The source which has been used the longest and for which we have the most information is adult bone marrow. Peripheral blood has also been used, but for the number of stem and progenitor cells from blood to be in high enough concentration to be of clinical efficiency, they need to be mobilized into the blood from the marrow after recovery from chemotherapy and/or after administration of growth factors. The most recent source of transplantable cells, until 1988 considered mainly discardable material, are those from the umbilical cord and placenta at the birth of a child. (2) This last source of cells is the focus of this brief review. Clinical Transplantation and Cord Blood Banking Since our original suggestion that cord blood could serve as a source of transplantable stem and progenitor cells, (2) which led to the first transplant using HLAmatched cord blood from a sibling (3) that successfully corrected the hematological and life-threatening manifestations of a genetic disorder, there have been well over 230 cord blood transplants done worldwide for an assortment of malignant and non-malignant disorders. (3-17) A listing of most of the disorders treated by sibling and unrelated cord blood transplantation is given in Table 1. This listing is not meant to be all inclusive as the author may not be aware of all the transplants done to date, and the rapidity with which cord blood is being used for transplantation suggests that new disorders will be evaluated with this source of stem/progenitor cells in the near future. Table 1: Disorders for which cord blood transplantation has been utilized as a treatment modality* Acute Lymphoid Leukemia - Remission, Relapse Acute Myeloid Leukemia - Remission, Relapse Chronic Myeloid Leukemia - Accelerated/Blastic Juvenile Chronic Myeloid Leukemia Myelodysplastic Syndrome Neuroblastoma Acute Megakaryocytic Thrombocytopenia Severe Combined Immunodeficiency Common Variable Immunodeficiency Wiskott-Aldrich Syndrome x-linked Lymphoproliferative Disease Hurler Syndrome Hunter Syndrome

2 Fanconi Anemia Severe Aplastic Anemia β-thalassemia Sickle Cell Anemia Lesch-Nyhan Syndrome Pure Red Cell Aplasia Osteopetrosis Globoid Cell Leukodystrophy Adrenoleukodystrophy Günther s Disease - Porphyrin Accumulation LAD Syndrome - Adhesive membrane Glycoprotein Deficiency Kostmann s Syndrome Diamond Blackfan * This is not meant to be an inclusive list. There may be other disorders treated by cord blood transplantation that the author is not aware of. The first transplant took place in October 1988, (3) and the child is well more than seven years after the transplant. That first cord blood transplant, as well as the first five done and a total of seven of the first ten transplants done, utilized cord blood that had been sent from a distant obstetrical unit to the author s laboratory, where they were tested for viability, number and proliferative capacity of granulocyte-macrophage (CFU-GM), erythroid (BFU-E), and multipotential (CFU-GEMM) progenitors, frozen, and stored cryopreserved until they were hand-delivered to the center where the transplants were done. (3-6) These centers included Paris, France; Cincinnati, Ohio; Baltimore, Maryland; and Minneapolis, Minnesota. The first cord blood bank was established in the author s laboratory. It was the later establishment of unrelated cord blood banks, in particular the one at the New York Blood Center from which a very large proportion of the unrelated cord blood transplant donor cells have come, that confirmed for unrelated cells (16,17) the low graft-versus-host disease (GVHD) originally noted with sibling cells (3-15) and that led to the first cord blood transplants for adults. While there have been a good number of clinical papers written on the experience of using sibling cells in the context of children as recipients,3-15 information has only recently begun to accumulate that relates the experience of centers doing transplants with unrelated cells for adult recipients who are of higher body weight. (16,17) Recipients of up to 80 Kg body weight have thus far been engrafted with unrelated donor cells, and patients in their thirties and forties have served as recipients with engraftment noted (J. Kurtzberg & P. Rubinstein, personal communications). The engraftment rates for sibling and unrelated cord blood transplants have been in the greater than ninety percent range, and GVHD, even using unrelated cells, has been relatively mild compared to use of similarly mismatched unrelated bone marrow donor cells. The GVHD seen in these circumstances has been, so far, easy to manage. This lowered amount of GVHD has not been associated with a higher level of relapse thus far when cord blood cells have been used to treat patients with leukemia. The rate at which cord blood has been used for transplantation has accelerated greatly. In 1988 and 1989, a total of only two cord blood transplants had been done. With

3 the growth and utilization of samples from the New York Blood Center Unrelated Cord Blood Bank, and the establishment of a number of other unrelated cord blood banks in the United States, Europe, Australia, Thailand, Japan and elsewhere, the rate of cord blood transplants will increase, as will our knowledge of the broadness of applicability of these cells. In addition to the above banks, a number of commercial ventures into the storage of cord blood for autologous or family use have opened up. It is the author s opinion that the development of the field of cord blood transplantation will be enhanced by the simultaneous development of banks that store donated bloods to be used in an unrelated setting, as well as banks that store cord blood for directed donations for related or autologous use. Both are important types of banks necessary to anticipate the needs of the future. Unrelated banks may not have the money, resources or inclination to store directed donations for an affected sibling or relative, and not all recipients in need of a transplant may find the appropriate HLA type of cord blood from an unrelated bank. As far as banking of autologous cells is concerned, the most perfectly matched set of cells for oneself is one s own cells. There are certainly enough births in the world to satisfy collections of cord blood for both unrelated and related/autologous banks. Most of the cord blood transplants done have utilized cryopreserved samples. While clinical experience with cryopreserved cord blood has been limited to use of cells frozen from weeks to a few years, theoretically, once cells have been frozen, and assuming no problems with the freezing methodology and with liquid nitrogen storage tanks, cells should remain in cryopreserved form for at least the lifetime of an individual. Our recent studies have demonstrated very high efficiency recovery of viable immature and mature subsets of CFU-GM, BFU-E and CFU-GEMM with high proliferative capacity from cord blood stored frozen for up to ten years.18 This recovery was similar to that of these same cells assessed after only a few weeks of storage. (2,19) There may still be information to be learned regarding the biophysics and biology of cryopreservation and efforts in this area of research could be rewarding. Cord blood stored frozen in a relatively unseparated form can be thawed and retrieved in viable form and further purified, transduced by retroviral vectors with new genetic material, and expanded ex vivo for more mature stem cells and for immature and mature subsets of progenitor cells. (20) Additionally, purified cord blood stem and progenitor cells can be frozen and recovered in viable form.21 Autologous cord blood transplants have thus far been done only in the context of gene therapy using non-cryopreserved cells. (22,23) Three patients, diagnosed in utero with adenosine deaminase (ADA)-deficient severe combined immunodeficiency (SCID), had their cord blood collected at birth, separated for CD34+ cells by column maneuvers, preincubated with a combination of growth factors and subsequently with retroviral vectors containing a normal ADA-gene, and then reinfused into the patients after a number of days. While it is too early to determine if this procedure has resulted in therapeutic benefit, it is clear that a small but significant number of the infused cells in these patients carry ADA-transduced genes. (22) The patients have been on pegylated ADA since birth, and most recently, decreasing the infusion of pegylated ADA has been coincident with a increase in the percentage and numbers of cells that express the transduced ADA-gene. (23)

4 Biology of Cord Blood Stem and Progenitor Cells Cord blood is enriched for hematopoietic stem and progenitor cells with high levels of proliferative, replating and expansion capacity in vitro. (2,19,20,24) These cells can be phenotypically characterized by cell surface markers as being CD34+++, CD38- and thy1+. These cells are mainly in a slowly cycling or resting condition with a prolonged G1 phase of the cell cycle and are insensitive to kill by pulse-treatment of the cells with high specific activity tritiated thymidine. However, these immature cells respond rapidly to stimulation of their proliferation with growth factors such as GM-CSF, G-CSF, IL-3 and erythropoietin in combination with potent co-stimulating molecules such as steel factor or the Flt3/Flk-2-ligand. Cord blood plasma is a rich source of known, as well as uncharacterized, growth factors, (25) but how these interrelate to regulate the growth of immature cord blood cells is not known. Well over 50 cytokines are now known to regulate the proliferation of hematopoietic stem and progenitor cells, at least in vitro; (26) some have direct action, others act indirectly by inducing the release of cytokines from accessory cells. Many of these cytokines have pleiotropic and what appear to be redundant activities. (26) It will probably be a while before we fully understand this interacting network of cytokine-cell interactions and which of these cytokines may be of more relevance physiologically. However, it is already clear that combinations of cytokines can be used to good advantage to expand hematopoietic stem and progenitor cells from cord blood ex vivo. (19,24,25) Unfortunately, whether or not those stem cells can be maintained or expanded by these ex vivo maneuvers has been hindered for all tissue sources of these earliest cells because no assay yet exists that can definitively recognize these long-term marrow repopulating stem cells from humans and quantitate them. The earliest human cell that can be quantitated is the long-term culture initiating cell, but it has not been demonstrated that this defines the long-term marrow repopulating cell. For this reason, a number of groups have begun using SCID mice, (27) transgenic SCID mice that express human GM-CSF, IL-3 and steel factor, (28) or non-obese diabetic (NOD) SCID mice (28) as possible in vivo models for detection and quantitation of candidate longterm marrow repopulating human stem cells. Immunology and Cord Blood Cells In order to understand what might be responsible for the apparently low levels of GVHD noted after cord blood transplantation, a number of groups (including our own) have begun to evaluate the immunological reactivity of cord blood lymphocytes and natural killer cells. (29-31) Laboratory studies that might, at least in part, explain lowered GVHD reflect lowered levels of cytotoxic T-cell activity generated from cord blood T- cells in response to primary, secondary and tertiary allogeneic cell stimulation (29) and the induction of a state of unresponsiveness of proliferation of cord blood T-cells after priming with alloantigen. (30) Of interest is that natural killer cell activity in cord blood is low, due to functional and phenotypic immaturity of these cells, but these cells do respond well to stimulation of killing activity by IL-2 and IL-12. (31) In-depth analysis of the mechanisms responsible for differences between adult and cord blood T-lymphocytes

5 and natural killer cells remains to be evaluated and could prove useful to our understanding of immune activity. Gene Transfer into Cord Blood Stem and Progenitor Cells Cord blood stem and progenitor cells are efficiently transduced with new genetic material by using either retroviral (32,33) or recombinant adeno-associated viral (AAV) vectors. (34) Much more information is known about the use of retroviral, compared with AAV, vectors, and it is still to be decided whether AAV vectors stably integrate into the genome, or if in fact this is mainly episomal and transient. In addition to adding genes to correct genetic disorders, a potential future use might be to add genes that code for cytokine or cytokine receptors to stem and progenitor cells. Genes for the erythropoietin- 35 and IL-9-36 receptors have been transduced into cord blood progenitors at the level of a single isolated CD34+++ cell in the absence and presence of combinations of growth factors including erythropoietin and IL-9. At this single cell level, enhanced detection of erythroid and multipotential colonies with an erythroid component was seen in cells transduced with the erythropoietin35- or IL-936-receptor genes when erythropoietin or IL-9 was added. This erythroid differentiation was even more apparent when cells were transduced with both receptor genes36 and low levels of erythropoietin and IL-9 were added to the wells. A future use for such transduction may be in the enhanced differentiation or expansion of certain more lineage-restricted cells in vivo or in vitro. However, whether this would be at the expense of self-renewal would have to be determined. Conclusion The field of cord blood transplantation is expanding rapidly. Cord blood banking is beginning to provide an addition or alternative to bone marrow registries. Currently, cord blood banks are extremely valuable when the appropriate HLA-types cannot be found in bone marrow registries or when a transplantation is needed immediately. Bone marrow registries can take months to identify a donor while banked cord blood is immediately available for use. While we have much to learn regarding the full range of the therapeutic benefits inherent in cord blood, it is anticipated that at some time in the not too distant future most individuals needing a transplant as treatment for a cancer or genetic disorder will be able to have one through either unrelated, related or autologous cord blood banks. Manipulation of cord blood cells for expansion, so that one sample will always be enough for one and perhaps numerous recipients seems possible; this possibly could be greatly accelerated if we had at hand a quantitative assay for the human longterm marrow repopulating stem cell. The correction of genetic defects by transfer of a new or normal gene is only just beginning to be evaluated clinically, and it is anticipated that cord blood will be a vehicle of choice for such correction in the future. Additionally, a greater understanding of gene transduction into early quiescent stem cells in cord blood may increase the possibilities for creative ideas for manipulation and modulation of the proliferative, self-renewal and differentiation of stem cells. The future for cord blood transplantation continues to look bright.

6 Acknowledgments: I thank Rebecca Miller for typing the manuscript. The author is supported by US Public Health Service Grants R01 HL56416, R01 HL54037, and a project in P01 HL53586 from the NHLBI of the NIH. Previous studies based on some of the work referred to herein were supported by grants R37 CA36464 and R01 HL46549 from the NCI and NIH. References 1. Lu L, Shen RN, Broxmeyer HE: Stem cells from bone marrow, umbilical cord blood and peripheral blood for clinical application: Current status and future applications. Crit Review Oncology/Hematol 22:61, Broxmeyer HE, Douglas GW, Hangoc G, Cooper S, Bard J, English D, Arny M, Thomas L, Boyse EA: Human umbilical cord blood as a potential source of transplantable hematopoietic stem/progenitor cells. Proc Natl Acad Sci USA 86:3828, Gluckman E, Broxmeyer HE, Auerbach AD, Friedman HS, Douglas GW, Devergie A, Esperou H, Thierry D, Socie G, Lehn P, Cooper S, English D, Kurtzberg J, Bard J, Boyse EA: Hematopoietic reconstitution in a patient with Fanconi s anemia by means of umbilical-cord blood from an HLA-identical sibling. New Engl J Med 321:1174, Wagner JE, Broxmeyer HE, Byrd RL, Zehnbauer B, Schmeckpeper B, Shah N, Griffin C, Emanuel PD, Zuckerman KS, Cooper S, Carow C, Bias W, Santos GW: Transplantation of umbilical cord blood after myeloablative therapy: analysis of engraftment. Blood 79:1874, Kohli-Kumar M, Shahidi NT, Broxmeyer HE, Masterson M, Delaat C, Sambrano J, Morris C, Auerbach AD, Harris RE: Haematopoietic stem/progenitor cell transplant in Fanconi anaemia using HLA-matched sibling umbilical cord blood cells. Brit J Haematol 85:419, Broxmeyer HE, Kurtzberg J, Gluckman E, Auerbach AD, Douglas G, Cooper S, Falkenburg JHF, Bard J, Boyse EA: Umbilical cord blood hematopoietic stem and repopulating cells in human clinical transplantation. Blood Cells 17:313, Bogdanic V, Nemet D, Kastelan A, Latin V, Petrovecki M, Brkljacic-Surlakovic L, Kerhin-Brkljacic V, Aurer I, Konja J, Mrsic M, Kalenic S, Labar B: Umbilical cord blood transplantation in a patient with Philadelphia chromosome-positive chronic myeloid leukemia. Transplantation 56:477, Vowels MR, Lam-Po-Tang R, Berdoukas V, Ford D, Thierry D, Purtilo D, Gluckman E: Brief Report: Correction of x-linked lymphoproliferative disease by transplantation of cord-blood stem cells. New Engl J Med 329:1623, Pahwa RN, Fleischer A, Than S, Good RA: Successful hematopoietic reconstitution with transplantation of erythrocyte-depleted allogeneic human umbilical cord blood cells in a child with leukemia. Proc Natl Acad Sci USA 91:4485, Kernan NA, Schroeder ML, Ciavarella D, Preti RA, Rubinstein P, O Reilly RJ: Umbilical cord blood infusion in a patient for correction of Wiskott Aldrich Syndrome. Blood Cells 20:245, 1994

7 11. Issaragrisil S, Visuthisakchai S, Suvatte V, Tanphaichitr VS, Chandanayingyong D, Schreiner T, Kanokpongsakdi S, Siritanaratkul N, Piankijagum A: Brief report: Transplantation of cord-blood stem cells into a patient with severe thalassemia. New Eng J Med 332:367, Kurtzberg J, Graham M, Casey J, Olsen J, Stevens C, Rubinstein P: The use of umbilical cord blood in mismatched related and unrelated hemopoietic stem cell transplantation. Blood Cells 20:275, Vilmer E, Sterkers G, Rahimy C, Denamur E, Elion J, Broyart A, Lescoeur B, Tiercy JM, Gerota J, Blot P: HLA mismatched cord blood transplantation in a patient with advanced leukemia. Transplantation 53:1128, Brichard B, Vermylen C, Ninane J, Cornu G: Persistence of fetal hemoglobin production of successful transplantation of cord blood stem cells in a patient with sickle cell anemia. J Ped 128:241, Wagner JE, Kernan NA, Steinbuch M, Broxmeyer HE, Gluckman E: Allogeneic sibling umbilical cord blood transplantation in forty-four children with malignant and non-malignant disease. Lancet 346:214, Kurtzberg J, Laughlin M, Graham ML, Smith C, Olson JF, Casey JR, Halperin ED, Ciocci G, Carrier C, Stevens CE, Rubinstein P: Single center transplantation of HLAmatched and partially mismatched unrelated placental bloodñan alternative source of hemopoietic stem cells for bone marrow transplantation. N Engl J Med, in press, Wagner JE, Rosenthal J, Sweetman R, Shu XO, Davies SM, Ramsay NKC, McGlave PB, Sender L, Cairo MS. Successful transplantation of HLA-matched and HLAmismatched umbilical cord blood from unrelated donors: analysis of engraftment and acute graft-versus-host-disease. N Engl J Med, in press, Broxmeyer HE, Cooper S: High recovery of immature hematopoietic progenitor cells with extensive proliferative capacity from human cord blood cryopreserved for 10 years. Clin and Exp Immunol, in press, Broxmeyer HE, Hangoc G, Cooper S, Ribeiro RC, Graves V, Yoder M, Wagner J, Vadhan-Raj S, Rubinstein P, Broun ER: Growth characteristics and expansion of human umbilical cord blood and estimation of its potential for transplantation of adults. Proc Natl Acad Sci USA 89:4109, Lu L, Ge Y, Li ZH, Freie B, Clapp DW, Broxmeyer HE: CD34+++ stem/progenitor cells purified from cryopreserved normal cord blood can be transduced with high efficiency by a retroviral vector and expanded ex vivo with stable integration and expression of Fanconi anemia complementation C gene. Cell Transplantation 4:493, Lu L, Li ZH, Broxmeyer HE: Recovery and characterization of CD34+ cord blood cells after cryopreservation. In Vivo, in press, Kohn DB, Weinberg KI, Nolta JA, Heiss LN, Lenarsky C, Crooks GM, Hanley ME, Annett G, Brooks JS, El-Khoureiy A, Lawrence K, Wells S, Moen RC, Bastian J, Williams-Herman DE, Elder M, Wara D, Bowen T, Hershfield MS, Mullen CA, Blaese RM, Parkman R: Engraftment of gene-modified umbilical cord blood cells in neonates with adenosine deaminase deficiency. Nature Medicine 10:1, 1995

8 23. Kohn DB, Weinberg KI, Lenarsky C, Crooks GM, Heiss LN, Nolta JA, Smogorzewska EM, Bastian J, Wara D, Elder M, Bowen T, Hershfield M, Blaese RM, Parkman R: Selective accumulation of ADA gene-transduced T-lymphocytes upon Peg-ADA dosage reduction after gene therapy with transduced CD34+ umbilical cord blood cells. Blood 86 (Suppl 1):295a, 1995 (abstr) 24. Broxmeyer HE: Cord blood, an alternative source for stem and progenitor cell transplantation. Current opinion in Pediatrics. Hematology and Oncology Section. Philadelphia, Current Science, 7:47, Ruggieri L, Heimfeld S, Broxmeyer HE: Cytokine-dependent ex vivo expansion of early subsets of CD34+ cord blood myeloid progenitors is enhanced by cord blood plasma, but expansion of the more mature subsets of progenitors is favored. Blood Cells 20:436, Broxmeyer HE: Commentary: Is interleukin-17, an inducible cytokine that stimulates production of other cytokines, merely a redundant player in a sea of other biomolecules? J Exp Med, in press, Vormoor J, Lapidot T, Pflumio F, Risdon G, Patterson B, Broxmeyer HE, Dick J: Immature human cord blood progenitors engraft and proliferate to high levels in immune-deficient SCID mice. Blood 83:2489, Bock TA, Orlic D, Dunbar CE, Broxmeyer HE, Bodine DM: Improved engraftment of human hematopoietic cells in severe combined immunodeficient (SCID) mice carrying human cytokine transgenes. J Exp Med 182:2037, Risdon G, Gaddy J, Stehman FB, Broxmeyer HE: Proliferative and cytotoxic responses of human cord blood T-lymphocytes following allogeneic stimulation. Cell Immunol 154:14, Risdon G, Gaddy J, Horie M, Broxmeyer HE: Alloantigen priming induces a state of unresponsiveness in human cord blood T cells. Proc Natl Acad Sci USA 92:2413, Gaddy J, Risdon G, Broxmeyer HE: Cord blood natural killer cells are functionally and phenotypically immature but readily respond to IL-2 and IL-12. J Interferon and Cytokine Res 15:527, Moritz T, Keller DC, Williams DA: Human cord blood cells as targets for gene transfer: potential use in genetic therapies of severe combined immunodeficiency disease. J Exp Med 178:529, Lu L, Xiao M, Clapp DW, Li ZH, Broxmeyer HE: High efficiency retroviral mediated gene transduction into single isolated immature and replatable CD34+++ hematopoietic stem/progenitor cells from human umbilical cord blood. J Exp Med 178:2089, Zhou SZ, Cooper S, Kang LY, Ruggieri L, Heimfeld S, Srivastava A, Broxmeyer HE: Adeno-associated virus 2-mediated high efficiency gene transfer into immature and mature subsets of hematopoietic progenitor cells in human umbilical cord blood. J Exp Med 179:1867, Lu L, Ge Y, Li ZH, Keeble W, Kabat D, Bagby GC, Broxmeyer HE, Hoatlin ME: Influence of retroviral-mediated gene transduction of recombinant human erythropoietin receptor gene into single hematopoietic stem/progenitor cells from human cord blood on the growth of these cells. Blood 87:525, 1996

9 36. Lu L, Li ZH, Xiao M, Broxmeyer HE: Influence of retroviral-mediated gene transduction of both the recombinant human erythropoietin receptor and interleukin-9 receptor genes into single CD34+++CD33- or low cord blood cells on cytokine stimulated erythroid colony formation. Exp Hematol 24:347, 1996

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