Sensitivity of Colorectal Cancer to Arginine Deprivation Therapy is Shaped by Differential Expression of Urea Cycle Enzymes

Sci Rep. 2018 Aug 14;8(1):12096. doi: 10.1038/s41598-018-30591-7.

Abstract

Tumors deficient in the urea cycle enzymes argininosuccinate synthase-1 (ASS1) and ornithine transcarbamylase (OTC) are unable to synthesize arginine and can be targeted using arginine-deprivation therapy. Here, we show that colorectal cancers (CRCs) display negligible expression of OTC and, in subset of cases, ASS1 proteins. CRC cells fail to grow in arginine-free medium and dietary arginine deprivation slows growth of cancer cells implanted into immunocompromised mice. Moreover, we report that clinically-formulated arginine-degrading enzymes are effective anticancer drugs in CRC. Pegylated arginine deiminase (ADI-PEG20), which degrades arginine to citrulline and ammonia, affects growth of ASS1-negative cells, whereas recombinant human arginase-1 (rhArg1peg5000), which degrades arginine into urea and ornithine, is effective against a broad spectrum of OTC-negative CRC cell lines. This reflects the inability of CRC cells to recycle citrulline and ornithine into the urea cycle. Finally, we show that arginase antagonizes chemotherapeutic drugs oxaliplatin and 5-fluorouracil (5-FU), whereas ADI-PEG20 synergizes with oxaliplatin in ASS1-negative cell lines and appears to interact with 5-fluorouracil independently of ASS1 status. Overall, we conclude that CRC is amenable to arginine-deprivation therapy, but we warrant caution when combining arginine deprivation with standard chemotherapy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • Arginase / pharmacology
  • Arginase / therapeutic use
  • Arginine / antagonists & inhibitors*
  • Arginine / metabolism
  • Argininosuccinate Synthase / metabolism*
  • Cell Line, Tumor
  • Colon / pathology
  • Colorectal Neoplasms / drug therapy*
  • Colorectal Neoplasms / mortality
  • Colorectal Neoplasms / pathology*
  • Drug Interactions
  • Drug Synergism
  • Feasibility Studies
  • Female
  • Fluorouracil / pharmacology
  • Fluorouracil / therapeutic use
  • Follow-Up Studies
  • Humans
  • Hydrolases / pharmacology
  • Hydrolases / therapeutic use
  • Inhibitory Concentration 50
  • Kaplan-Meier Estimate
  • Male
  • Mice
  • Ornithine Carbamoyltransferase / metabolism
  • Oxaliplatin / pharmacology
  • Oxaliplatin / therapeutic use
  • Polyethylene Glycols / pharmacology
  • Polyethylene Glycols / therapeutic use
  • Recombinant Proteins / pharmacology
  • Recombinant Proteins / therapeutic use
  • Retrospective Studies
  • Treatment Outcome
  • Urea / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Recombinant Proteins
  • Oxaliplatin
  • Polyethylene Glycols
  • Urea
  • Arginine
  • Ornithine Carbamoyltransferase
  • Hydrolases
  • ARG1 protein, human
  • Arginase
  • ADI PEG20
  • Argininosuccinate Synthase
  • Fluorouracil