Hypoxia-related carbonic anhydrase IX expression is associated with unfavourable response to first-line therapy in classical Hodgkin's lymphoma

Histopathology. 2019 Apr;74(5):699-708. doi: 10.1111/his.13808. Epub 2019 Mar 10.

Abstract

Aims: The present study evaluates the impact of hypoxia-related carbonic anhydrase IX and XII isoenzyme expression as a basic adaptive mechanism to neutralise intracellular acidosis in classical Hodgkin's lymphoma (cHL).

Methods and results: Eighty-one primary biopsies and 15 relapsed tissue samples diagnosed with cHL were analysed for necrosis, CAIX and CAXII expression and cell proliferation to compare hypoxia-related histological and functional data with survival characteristics. Variable, but highly selective cell membrane CAIX expression could be demonstrated in Hodgkin-Reed-Sternberg (HRS) cells in 39 of 81 samples (48.1%), while virtually no staining presented in their microenvironment. In contrast, CAXII expression in HRS cells could be demonstrated in only 18 of 77 samples (23.4%), with significant stromal positivity (50 of 77, 64.9%). The CAIX+ positive phenotype was strongly associated with lymphocyte depletion (four of four, 100%) and nodular sclerosis (29 of 51, 56.9%) subtypes. CAIX/Ki-67 dual immunohistochemistry demonstrated suppressed cell proliferation in CAIX+ positive compared to CAIX- negative HRS cells (P < 0.001). Seventy-two months' progression-free survival (PFS) was significantly lower for the CAIX positive group (0.192) compared with the CAIX negative group (0.771) (P < 0.001), while the overall survival (OS) did not differ (P = 0.097).

Conclusion: Hypoxic stress-related adaptation - highlighted by CAIX expression - results in cellular quiescence in HRS cells, potentially contributing to the short-term failure of the standard chemotherapy in cHL.

Keywords: Hodgkin's lymphoma; adaptation; cell cycle; hypoxia; resistance; survival.

MeSH terms

  • Acidosis / enzymology
  • Antigens, Neoplasm / metabolism*
  • Biopsy
  • Carbonic Anhydrase IX / metabolism*
  • Cell Hypoxia
  • Cell Proliferation
  • Cohort Studies
  • Follow-Up Studies
  • Hodgkin Disease / drug therapy*
  • Hodgkin Disease / enzymology*
  • Hodgkin Disease / pathology
  • Humans
  • Immunohistochemistry
  • Isoenzymes
  • Kaplan-Meier Estimate
  • Lymph Nodes / diagnostic imaging
  • Lymph Nodes / enzymology
  • Lymph Nodes / pathology
  • Necrosis / diagnostic imaging
  • Neoplasm Recurrence, Local / enzymology
  • Neoplasm Recurrence, Local / pathology
  • Progression-Free Survival

Substances

  • Antigens, Neoplasm
  • Isoenzymes
  • CA9 protein, human
  • Carbonic Anhydrase IX