GSTM1 and GSTT1 double null genotypes determining cell fate and proliferation as potential risk factors of relapse in children with hematological malignancies after hematopoietic stem cell transplantation

J Cancer Res Clin Oncol. 2022 Jan;148(1):71-86. doi: 10.1007/s00432-021-03769-2. Epub 2021 Sep 9.

Abstract

Purpose: This study aimed to retrospectively evaluate the genetic association of null variants of glutathione S-transferases GSTM1 and GSTT1 with relapse incidence in children with hematological malignancies (HMs) undergoing busulfan (BU)- containing allogeneic hematopoietic stem cell transplantation (HSCT) and to assess the impact of these variants on BU-induced cytotoxicity on the immortalized lymphoblastoid cell lines (LCLs) and tumor THP1 GST gene-edited cell models.

Methods: GSTM1- and GSTT1-null alleles were genotyped using germline DNA from whole blood prior to a conditioning BU-based regimen. Association of GSTM1- and GSTT1-null variants with relapse incidence was analyzed using multivariable competing risk analysis. BU-induced cell death studies were conducted in GSTs- null and non-null LCLs and CRISPR-Cas9 gene-edited THP1 leukemia cell lines.

Results: Carrying GSTM1/GSTT1 double null genotype was found to be an independent risk factor for post-HSCT relapse in 86 children (adjusted HR: 6.52 [95% Cl, 2.76-15.42; p = 1.9 × 10-5]). BU-induced cell death preferentially in THP1GSTM1(non-null) and LCLsGSTM1(non-null) as shown by decreased viability, increased necrosis and levels of the oxidized form of glutathione compared to null cells, while GSTT1 non-null cells showed increased baseline proliferation.

Conclusion: The clinical association suggests that GSTM1/GSTT1 double null genotype could serve as genetic stratification biomarker for the high risk of post-HSCT relapse. Functional studies have indicated that GSTM1 status modulates BU-induced cell death. On the other hand, GSTT1 is proposed to be involved in baseline cell proliferation.

Trial registration: ClinicalTrials.gov NCT01257854.

Keywords: Acute leukemia; Busulfan resistance; Hematological malignancies; Hematopoietic stem cell transplantation; Null genotypes of glutathione S-transferases; Post-transplant relapse.

MeSH terms

  • Adolescent
  • Biomarkers, Tumor / genetics
  • Busulfan / therapeutic use
  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Child
  • Child, Preschool
  • Drug Resistance, Neoplasm / genetics
  • Female
  • Gene Deletion
  • Genetic Predisposition to Disease / genetics
  • Genotype
  • Glutathione / analysis
  • Glutathione / metabolism
  • Glutathione Transferase / genetics*
  • Hematologic Neoplasms / genetics*
  • Hematologic Neoplasms / pathology
  • Hematologic Neoplasms / therapy
  • Hematopoietic Stem Cell Transplantation
  • Humans
  • Infant
  • Leukemia / genetics*
  • Leukemia / pathology
  • Leukemia / therapy
  • Male
  • Neoplasm Recurrence, Local / genetics*
  • Retrospective Studies
  • Risk Factors

Substances

  • Biomarkers, Tumor
  • glutathione S-transferase T1
  • Glutathione Transferase
  • glutathione S-transferase M1
  • Busulfan
  • Glutathione

Associated data

  • ClinicalTrials.gov/NCT01257854