bims-polyam Biomed News
on Polyamines
Issue of 2022‒05‒15
nine papers selected by
Sebastian J. Hofer
University of Graz


  1. FASEB J. 2022 May;36 Suppl 1
      Polyamines are vital for cellular life. Polyamines such as putrescine, spermidine, and spermine regulate the essential cellular process, including gene expression and cell proliferation. Given its cellular role, polyamine concentration in cells is tightly controlled. However, aberrant polyamine metabolism is associated with numerous diseases, including cancer. Growing evidence suggests that elevated polyamine levels are the absolute requirement for tumor growth and progression. The concentrations of cellular polyamines are controlled by the polyamine regulatory circuit comprising three different proteins: Ornithine Decarboxylase (ODC), Ornithine Decarboxylase Antizyme (OAZ), and Antizyme Inhibitor (AZIN). While ODC is directly involved in polyamine biosynthesis, OAZ and AZIN regulate the ODC activity via protein-protein interactions. The dysregulation of ODC, OAZ, and AZIN leads to elevated polyamines in numerous pathologies, making them attractive targets to control polyamine levels. Besides regulating polyamine synthesis, OAZ is believed to modulate polyamine transport via multiple pathways. However, the precise mechanism of OAZ-mediated polyamine regulation outside of the polyamine biosynthetic pathway remains elusive. We hypothesize that OAZ sequestration results in increased polyamine uptake. To provide evidence to our hypothesis, we generated covalent OAZ-mimetic inactivators targeting both ODC and AZIN. Using biochemical experiments, we demonstrate that these OAZ-mimetics inhibit the activity of ODC and prevent the sequestration of OAZ by AZIN. Using Mass spectrometric experiments, we determine the covalent binding of OAZ-mimetics to both ODC and AZIN. We employ a novel gel assay to assess the rate of covalent modification of ODC and AZIN. Finally, using computational modeling, we determine the mode of binding of OAZ-mimetics to both ODC and AZIN to provide insights into inhibition mechanisms.
    DOI:  https://doi.org/10.1096/fasebj.2022.36.S1.0R326
  2. FASEB J. 2022 May;36 Suppl 1
      Breast cancer (BC) is the second leading cause of death in women. Co-existence of diabetes and BC, termed diabetic BC, can be lethal, leading to higher mortality (15-40%) than BC alone. In triple negative breast cancer (TNBC) patients, chance of TNBC recurrence is about 3 months, and chance of mortality can be as high as 75%. TNBC is highly refractive, heterogenous, and resistant to most chemotherapies. Polyamines, which are ubiquitous in most cells, and play a role in cell growth, have been shown to be elevated in cancer, though their role in diabetic BC has not been explored. We hypothesized that high glucose/diabetic conditions increase TNBC cell proliferation through modification of the enzymes (ornithine decarboxylase and spermine oxidase) in the polyamine pathway. The objective was to determine potential targets in the polyamine pathway to mitigate TNBC advancement in diabetic conditions. For this purpose, MDA-MB-231 (TNBC) and MCF10-A (normal breast epithelial) cell lines were used. Both were treated with low (5mM) and high glucose (25mM) concentrations and effects on polyamine levels, polyamine enzyme, and cell proliferation were monitored. Polyamine levels were assayed using reverse phase high performance liquid chromatography. Cell proliferation was assessed using a fluorescence-based assay, and polyamine enzyme expression was monitored at the mRNA and protein level using RT-PCR and Western Blots. Samples were sent to Johns Hopkins University for polyamine enzyme activity analysis. Further, an approved inhibitor of polyamine synthesis, alpha-difluoromethylornithine (a-DFMO, 5mM) was used in combination with glucose treatments. Under diabetic/high glucose conditions, putrescine levels were elevated in MDA-MB-231 cells (135%), which correlated with higher cell proliferation (123%). Polyamine enzyme activity of ODC increased (from ~75 pMolCO2/hr/mg protein to ~150 pMolCO2/hr/mg protein) and SMOX decreased (from ~0.4 pMolH202/min/mg protein to ~0.06 pMolH202/min/mg protein) in concert with changes observed at protein levels with high glucose exposure. DFMO was effective in reducing polyamine levels and cell proliferation, however re-supplementation of polyamines (spermidine and spermine) restored cell proliferation to that, indicating that DFMO is only cytostatic. MCF-10A cells showed marked elevation in cell proliferation with high glucose. DFMO prevented this increase; however no apparent change was observed in polyamine levels. The polyamine biosynthetic enzymes (ornithine decarboxylase and spermine oxidase) play an active role in increasing cell proliferation under high glucose conditions in TNBC. Since DFMO caused only cytostatic effects, there is a need for a more targeted approach to regulate polyamine levels and mitigate TNBC growth under diabetic conditions.
    DOI:  https://doi.org/10.1096/fasebj.2022.36.S1.R4686
  3. Int J Mol Sci. 2022 Apr 21. pii: 4614. [Epub ahead of print]23(9):
      The polyamines, spermine (Spm) and spermidine (Spd), are important for cell growth and function. Their homeostasis is strictly controlled, and a key downregulator of the polyamine pool is the polyamine-inducible protein, antizyme 1 (OAZ1). OAZ1 inhibits polyamine uptake and targets ornithine decarboxylase (ODC), the rate-limiting enzyme of polyamine biosynthesis, for proteasomal degradation. Here we report, for the first time, that polyamines induce dimerization of mouse recombinant full-length OAZ1, forming an (OAZ1)2-Polyamine complex. Dimerization could be modulated by functionally active C-methylated spermidine mimetics (MeSpds) by changing the position of the methyl group along the Spd backbone-2-MeSpd was a poor inducer as opposed to 1-MeSpd, 3-MeSpd, and Spd, which were good inducers. Importantly, the ability of compounds to inhibit polyamine uptake correlated with the efficiency of the (OAZ1)2-Polyamine complex formation. Thus, the (OAZ1)2-Polyamine complex may be needed to inhibit polyamine uptake. The efficiency of polyamine-induced ribosomal +1 frameshifting of OAZ1 mRNA could also be differentially modulated by MeSpds-2-MeSpd was a poor inducer of OAZ1 biosynthesis and hence a poor downregulator of ODC activity unlike the other MeSpds. These findings offer new insight into the OAZ1-mediated regulation of polyamine homeostasis and provide the chemical tools to study it.
    Keywords:  antizyme; dimerization; ornithine decarboxylase; polyamine analogues; polyamine uptake; polyamines; ribosomal frameshifting; α-difluoromethylornithine
    DOI:  https://doi.org/10.3390/ijms23094614
  4. FASEB J. 2022 May;36 Suppl 1
      The polyamines putrescine, spermidine and spermine are organic polycations that regulate many cell functions including proliferation and differentiation. It is known that certain genes of the polyamine system are dysregulated after kidney ischemia reperfusion injury. Here we examined the hypothesis that different forms of acute and chronic kidney injury lead to similar changes in the expression patterns of the polyamine system. In different models of acute and chronic kidney injury expression of genes involved in polyamine homeostasis were analyzed by RT-qPCR and RNAScope. In these models, expression of catabolic enzymes (Aoc1 and Sat1) was upregulated, and the anabolic enzymes (Odc1, Sms) were downregulated. The putrescine-degrading enzyme AOC1 exhibits the most striking changes. Interestingly, it can act together with ODC1 as gatekeepers of the polyamine system. The detected increase of Aoc1 takes place in the injured but regenerating proximal tubules. As a screening for stimuli of increased Aoc1 expression, we used mouse embryonic kidney explants. Here we observed changes of Aoc1expression under hypoxia and hyperosmotic conditions. These changes were further examined in mouse models of hypoxia. However, in vivo, hypoxia did not lead to changes of Aoc1 expression. Hyperosmolarity was confirmed as a stimulus by using the kidney cell lines M15 and 209/MDCT as well as cultured primary proximal tubules. Using reporter gene and RNA-stability assays, we could show that the increase in Aoc1 expression is based on mRNA-stabilization and transcriptional activation of one certain isoform. The activated isoform contains an additional set of 22 amino acids N-terminally that lead to an altered subcellular localization. In conclusion, different models of kidney injury exhibit a similar pattern of dysregulation of the polyamine system with the most striking change being the upregulation of Aoc1 in proximal tubules. Using hyperosmolarity as a stimulus, we provide first insights into the regulation of Aoc1 under harmful conditions.
    DOI:  https://doi.org/10.1096/fasebj.2022.36.S1.R3345
  5. Int J Mol Sci. 2022 Apr 25. pii: 4734. [Epub ahead of print]23(9):
      L-Arginine:glycine amidinotransferase (AGAT) catalyzes the formation of L-homoarginine (hArg) and L-ornithine (Orn) from L-arginine (Arg) and L-lysine (Lys): Arg + Lys ↔ hArg + Orn; equilibrium constant KhArg. AGAT also catalyzes the formation of guanidinoacetate (GAA) and Orn from Arg and glycine (Gly): Arg + Gly ↔ GAA + Orn; equilibrium constant KGAA. In humans, pharmacological hArg is metabolized to Lys. Low circulating and low excretory concentrations of hArg are associated with worse outcomes and mortality in the renal and cardiovascular systems. The metabolism and pharmacology of hArg have been little investigated. In the present study, we investigated the effects of pharmacological hArg (i.p., 0, 20, 220, 440 mg/kg at time point 0 min) on amino acids homeostasis in a rat model of isoprenaline-induced takotsubo cardiomyopathy (i.p., 50 mg/kg at time point 15 min). We measured by gas chromatography-mass spectrometry free and proteinic amino acids, as well as the polyamines putrescine and spermidine in the heart, lung, kidney, and liver of ten rats sacrificed at various time points (range, 0 to 126 min). hArg administration resulted in multiple changes in the tissue contents of several free and proteinic amino acids, as well as in the putrescine-spermidine molar ratio, an indicator of polyamines catabolism. Our results suggest that Lys and Arg are major metabolites of pharmacological hArg. Kidneys and heart seem to play a major metabolic role for hArg. Circulating Lys does not change over time, yet there is a considerable interchange of free Lys between organs, notably kidney and heart, during the presence of isoprenaline in the rats (time range, 15 to 90 min). Antidromic changes were observed for KhArg and KGAA, notably in the heart in this time window. Our study shows for the first time that free hArg and sarcosine (N-methylglycine) are positively associated with each other. The acute effects of high-dosed hArg administration and isoprenaline on various amino acids and on AGAT-catalyzed reaction in the heart, lung, kidney, and liver are detailed and discussed.
    Keywords:  AGAT; GC-MS; L-arginine; L-homoarginine; L-lysine; amino acids; isoprenaline; polyamines; putrescine; sarcosine; spermidine
    DOI:  https://doi.org/10.3390/ijms23094734
  6. Int J Biol Sci. 2022 ;18(7): 3034-3047
      5'-Methylthioadenosine phosphorylase (MTAP) is a key enzyme in the methionine salvage pathway and has been reported to suppress tumorigenesis. The MTAP gene is located at 9p21, a chromosome region often deleted in breast cancer (BC). However, the clinical and biological significance of MTAP in BC is still unclear. Here, we reported that MTAP was frequently downregulated in 41% (35/85) of primary BCs and 89% (8/9) of BC cell lines. Low expression of MTAP was significantly correlated with a poor survival of BC patients (P=0.0334). Functional studies showed that MTAP was able to suppress both in vitro and in vivo tumorigenic ability of BC cells, including migration, invasion, angiogenesis, tumor growth and metastasis in nude mice with orthotopic xenograft tumor of BC. Mechanistically, we found that downregulation of MTAP could increase the polyamine levels by activating ornithine decarboxylase (ODC). By treating the MTAP-repressing BC cells with specific ODC inhibitor Difluoromethylornithine (DFMO) or treating the MTAP-overexpressing BC cells with additional putrescine, metastasis-promoting or -suppressing phenotype of these MTAP-manipulated cells was significantly reversed, respectively. Taken together, our data suggested that MTAP has a critical metastasis-suppressive role by tightly regulating ODC activity in BC cells, which may serve as a prominent novel therapeutic target for advanced breast cancer treatment.
    Keywords:  Breast cancer; MTAP; Metastasis; ODC; Polyamine biosynthesis
    DOI:  https://doi.org/10.7150/ijbs.67149
  7. Int J Mol Sci. 2022 Apr 19. pii: 4472. [Epub ahead of print]23(9):
      Soil salinization has become a serious challenge to modern agriculture worldwide. The purpose of the study was to reveal salt tolerance induced by spermine (Spm) associated with alterations in water and redox homeostasis, photosynthetic performance, and global metabolites reprogramming based on analyses of physiological responses and metabolomics in creeping bentgrass (Agrostis stolonifera). Plants pretreated with or without 0.5 mM Spm were subjected to salt stress induced by NaCl for 25 days in controlled growth chambers. Results showed that a prolonged period of salt stress caused a great deal of sodium (Na) accumulation, water loss, photoinhibition, and oxidative damage to plants. However, exogenous application of Spm significantly improved endogenous spermidine (Spd) and Spm contents, followed by significant enhancement of osmotic adjustment (OA), photosynthesis, and antioxidant capacity in leaves under salt stress. The Spm inhibited salt-induced Na accumulation but did not affect potassium (K) content. The analysis of metabolomics demonstrated that the Spm increased intermediate metabolites of γ-aminobutyric acid (GABA) shunt (GABA, glutamic acid, and alanine) and tricarboxylic acid (TCA) cycle (aconitic acid) under salt stress. In addition, the Spm also up-regulated the accumulation of multiple amino acids (glutamine, valine, isoleucine, methionine, serine, lysine, tyrosine, phenylalanine, and tryptophan), sugars (mannose, fructose, sucrose-6-phosphate, tagatose, and cellobiose), organic acid (gallic acid), and other metabolites (glycerol) in response to salt stress. These metabolites played important roles in OA, energy metabolism, signal transduction, and antioxidant defense under salt stress. More importantly, the Spm enhanced GABA shunt and the TCA cycle for energy supply in leaves. Current findings provide new evidence about the regulatory roles of the Spm in alleviating salt damage to plants associated with global metabolites reprogramming and metabolic homeostasis.
    Keywords:  antioxidant capacity; energy metabolism; ions homeostasis; metabolic pathway; osmotic adjustment; polyamines
    DOI:  https://doi.org/10.3390/ijms23094472
  8. FASEB J. 2022 May;36 Suppl 1
      This study was performed to screen a number of potentially life-extending supplements, including inhibitors of the TOR signal transduction pathway, while confirming life extension by other, previously tested compounds. This initial screen was conducted in male flies of a comparatively long-lived y w strain of D. melanogaster. A hypothesis was that reports of life extension by some compounds would be confirmed and other longevity-enhancing compounds would be identified, with optimum dosages that could be tested subsequently in males and females of multiple genotypes. The following supplements were delivered continuously throughout adult life, beginning 2 d posteclosion: rapamycin (0.1, 0.5, 1, 10, 100, 200 and 400 µM), spermidine (10 µM - 10 mM), LY294002 (100 nM - 10 µM), wortmannin, KU0063794 and PX-866-17OH (all 1 nM - 10 µM), AZD8055, PI-103 HCl and Torin 2 (all 100 pM - 10 µM), WYE-28 and WYE-132 (both 10 pM - 1 µM) and DMSO solvent (0.02-0.2%). Unexpectedly, the main finding was a strong, dose-dependent decrease in mean life span at high doses of rapamycin, ranging from a 29% decrease at 100 µM to 46% decrease at 400 µM (all P < 0.0005). Rapamycin had no significant effect at the lower doses. The highest dose of wortmannin (10 μM) also drastically decreased longevity (73%, P < 0.0005) and the highest dose of spermidine (10 mM) had a smaller adverse effect (11%, P < 0.0005), while the highest doses of PI-103 HCl (10 μM) and AZD8055 (10 μM), an intermediate dose of AZD8055 (0.1 μM) and the lowest dose of WYE-132 (10 pM) increased life span by 4-6% (P = 0.001 - 0.029). The other supplements had no significant effect on longevity at any dose. Possible explanations of the rapamycin result include use of a DMSO solvent in contrast to ethanol used for past studies, or storage of DMSO-solubilized rapamycin in aliquots at -20ºC; however, the DMSO solvent at the low concentrations used to dissolve the supplements had no effect on life span. Experiments are in progress to test the effects of high dose rapamycin in male and female flies of several strains, comparing ethanol and DMSO solvents, different food recipes, lighting and storage conditions. A current conclusion is that rapamycin is not universally beneficial in Drosophila and that inhibitors of various kinases at the doses studied have limited or no effect on longevity.
    DOI:  https://doi.org/10.1096/fasebj.2022.36.S1.R3257
  9. FASEB J. 2022 May;36 Suppl 1
      INTRODUCTION: Understanding and identifying differences in biological processes between males and females are critical for developing the sex-based treatments for diseases. Mitochondrial dysfunction has been implemented in various kidney diseases yet baseline mitochondrial function and related sex differences within the kidney are not well established. Our previous data obtained in isolated renal mitochondria showed higher oxygen consumption and overall antioxidant capacity, and attenuated mitochondrial permeability transition in males. There is a pressing need for a more complete understanding of normal kidney function; to close this gap in knowledge, we hypothesized that divergent metabolic processes may influence the differences in mitochondrial bioenergetics and antioxidant capacity that we have previously identified.METHODS: Tissues were isolated from the kidneys collected from male and female Sprague Dawley (SD) rats at 11 weeks of age (Charles River labs, USA). The kidneys were perfused via the abdominal aorta with PBS/heparin solution to remove excess blood. Immediately following kidney collection, the cortex and medulla were isolated and snap frozen for metabolomic analysis. Metabolic profiles of renal cortices and medullae were generated using UHPLC-HRMS, and metabolites were identified by retention time exact mass using MAVEN and MetaboAnalyst software. Ingenuity Pathway Analysis (IPA) was used to visualize and identify pathways of interests.
    RESULTS: . A total of 174 mitochondria-focused metabolites were measured; to be considered significant, cutoffs of a 1.2 fold change (FC) with a corresponding p-value of 0.05 were used. In the renal cortex and medulla, respectively, 22 and 38 metabolites were identified as increased or decreased in males compared to the females. Initial analysis demonstrated clear stratification of metabolite groups between male and female samples, as well as cortical and medullary tissues. Females exhibited upregulated metabolites implicated in protein and nucleic acid synthesis pathways such as UDP-glucuronic acid (cortex/medulla, FC=1.796/1.615, p=0.013/<0.001), UDP-D-glucose (cortex/medulla, FC=1.415/1.594, p=<0.001/<0.001), guanosine(cortex/medulla, FC=1.290, p=0.018), and thymidine (cortex, FC=1.227, p=<0.001). Males, on the other hand, showed an upregulation of metabolites involved in the Kynurenine pathway (such as xanthurenic acid (cortex, FC=2.023, p=0.02), which is involved in NAD+ synthesis. Most interestingly, male kidneys also exhibited a major upregulation 5'-methylthioadenosine (MTA) compared to females in both the cortex and the medulla (cortex/medulla, FC=41.88/62.88, p=0.002/0.004). MTA is involved in the polyamine metabolism and spermine/spermidine signaling, known to have antioxidant properties and attenuate diabetic kidney disease and AKI.
    CONCLUSIONS: We report differences in metabolites in the cortex and medulla of young healthy male and female rats, primarily, related to their ability to utilize glucose and metabolize protein, and regulate spermine/spermidine pathway, which could explain differences in antioxidant capacity. The observed sex-related dissimilarities indicate that male and female kidneys at least partially rely on different metabolic pathways, which opens up opportunities to develop new renal disease treatments targeting males and females separately.
    DOI:  https://doi.org/10.1096/fasebj.2022.36.S1.R2556