Tippi MacKenzie, MD

Professor
Department of Surgery
+1 415 476-2538
Research Overview: 

Stem Cell Transplantation. Our lab studies in utero hematopoietic stem cell transplantation (IUHCT) with the goal of elucidating mechanisms of engraftment and tolerance induction. Transplantation of allogeneic stem cells into the early gestational fetus can overcome the limitations of postnatal bone marrow transplants, including rejection and graft vs host disease. We showed in a mouse model that maternal T cells are the main barrier to engraftment (PMC3026737), suggesting that IUHCT could be improved by transplanting maternal stem cells. We found that tolerance induction after IUHCT depends on both direct and indirect antigen presentation (PMC3668492) and is secondary to thymic deletion. In a mouse model, we improved engraftment with in utero depletion of fetal hematopoietic stem cells (by injecting an antibody against the cKit receptor) to increase the HSC niche for donor cell engraftment, with minimal toxicity (PMC4126335). Most recently, we demonstrated that IUHCT can result in engraftment of donor-derived microglia in the brain, which has important implications for the treatment of lysosomal storage disorders (PMID: 32102934).

Following these advances in the mouse model, we opened a Phase I clinical trial for IUHCT in patients with alpha thalassemia major (NCT02986698). Fetuses diagnosed with alpha thalassemia major receive hematopoietic stem cells that have been harvested from the mother, concomitantly with a blood transfusion to treat the fetal anemia. The hope is to induce tolerance to the maternal cells to allow the mother to be a viable donor for stem cell transplantation to treat the baby after birth. To date, two patients have completed the trial, both of whom safely received IUHCT and are now thriving toddlers!

Maternal-Fetal Tolerance. Our lab studies mechanisms of maternal-fetal tolerance with the goal of improving fetal intervention outcomes and preventing immune-mediated complications of pregnancy. During gestation, the fetus exists in a unique state of immune tolerance with the mother; we now understand that tolerance in both directions (maternal tolerance of the fetus (PMC4268439) and vice versa) is important for a healthy pregnancy. We have shown that in the context of preterm labor, the fetal immune system can be activated against maternal antigens, which triggers a cascade of events culminating in preterm uterine contractions (PMC6449052). We are now trying to understand changes in the microbiome (PMC7159194) and other antigens involved in this aberrant immune response so that we can develop targeted therapies for preterm birth. We are also fascinated by the role of congenital anomalies such as gastroschisis (PMC4977025, PMC6715406) in altering fetal immune development, with possible consequences on preterm birth and postnatal health.

Our lab is also investigating the role of autoimmune regulator gene (Aire) in supporting maternal-fetal tolerance. Aire prevents autoimmunity by inducing tolerance to self-antigens. A healthy pregnancy requires tolerance to a unique set of maternal self-antigens: those arising from the decidua, placenta, and embryo. We are investigating whether maternal self-tolerance to pregnancy-associated antigens protects a pregnancy and how the Aire gene may be involved. This work is relevant to common pregnancy complications such as miscarriage and intrauterine growth restriction, both of which are often associated with autoimmunity.

Fetal Molecular Therapies. Advances in molecular therapies such as gene therapy and gene editing have led to postnatal clinical trials aiming to treat congenital genetic diseases such as hemoglobinopathies, coagulopathies, neuromuscular degenerative diseases, and lysosomal storage disorders. Our team and collaborators are working toward applications of these therapies in the prenatal setting to treat fetuses with genetic diseases (PMC6453510).

The fetal environment offers multiple potential advantages over postnatal treatment for some congenital genetic diseases. First, the unique fetal immune environment may allow us to induce tolerance to a missing protein such as a clotting factor or a lysosomal enzyme. Second, it may be possible for systemically injected medication to reach cells in the fetal brain before the blood-brain barrier closes. Finally, fetal therapy may prevent organ-specific disease manifestations during a critical window of tissue development. A goal of the MacKenzie lab is to develop safe and effective fetal molecular therapies in translational animal models and to lead the way in developing responsible fetal molecular therapy clinical trials to treat patients with severe genetic diseases before birth.

Primary Thematic Area: 
Immunology
Secondary Thematic Area: 
Developmental & Stem Cell Biology
Research Summary: 
Stem cell transplantation, maternal-fetal tolerance, and fetal molecular therapies

Websites

Publications: 

In Utero Hematopoietic Stem Cell Transplantation for Fanconi Anemia.

Blood advances

Swartzrock L, Dib C, Denis M, Willner H, Ho K, Haslett E, Han J, Pan W, Byrne-Steele M, Brown B, Krampf MR, Girsen A, Blumenfeld YJ, El-Sayed YY, Roncarolo MGG, MacKenzie TC, Czechowicz AD

Dual α-globin and truncated EPO receptor knockin restores hemoglobin production in α-thalassemia-derived red blood cells.

bioRxiv : the preprint server for biology

Chu SN, Soupene E, Wienert B, Yin H, Sharma D, McCreary T, Jia K, Homma S, Hampton JP, Gardner JM, Conklin BR, MacKenzie TC, Porteus MH, Cromer MK

Prenatal AAV9-GFP administration in fetal lambs results in transduction of female germ cells and maternal exposure to virus.

Molecular therapy. Methods & clinical development

Borges B, Varthaliti A, Schwab M, Clarke MT, Pivetti C, Gupta N, Cadwell CR, Guibinga G, Phillips S, Del Rio T, Ozsolak F, Imai-Leonard D, Kong L, Laird DJ, Herzeg A, Sumner CJ, MacKenzie TC

Prenatal delivery of a therapeutic antisense oligonucleotide achieves broad biodistribution in the brain and ameliorates Angelman Syndrome phenotype in mice.

Molecular therapy : the journal of the American Society of Gene Therapy

Clarke MT, Remesal L, Lentz L, Tan DJ, Young D, Thapa S, Namduri S, Borges B, Kirn G, Valencia J, Lopez ME, Lu JH, Shiow LR, Dindot S, Villeda S, Sanders SJ, MacKenzie TC