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. 2024 Feb 15;19(2):e0298981.
doi: 10.1371/journal.pone.0298981. eCollection 2024.

Bioenergetic profiles of peripheral mononuclear cells and systemic inflammation in women with Interstitial Cystitis/Bladder Pain Syndrome (IC/BPS)

Parveen Kumar  1 , Robert A Oster  2 , Dean G Assimos  1 , Timothy J Ness  3 , Tanecia Mitchell  1
Affiliations

Bioenergetic profiles of peripheral mononuclear cells and systemic inflammation in women with Interstitial Cystitis/Bladder Pain Syndrome (IC/BPS)

Parveen Kumar et al. PLoS One. .

Abstract

Inflammation is thought to contribute to the etiology of interstitial cystitis/bladder pain syndrome (IC/BPS). It is well-known that disruption in metabolism in immune cells contributes to inflammation in several inflammatory diseases. The purpose of this study was to investigate whether cellular bioenergetics is altered in monocytes and lymphocytes from women with IC/BPS, and if these alterations correlate with systemic inflammatory markers. Age and BMI matched adult healthy women (HS; n = 18) and women with IC/BPS (n = 18) were included in the study. Blood was collected to assess cellular bioenergetics in monocytes and lymphocytes using a Seahorse XF96 Analyzer and plasma cytokine levels were measured using Meso Scale Discovery immunoassays. The correlation between bioenergetic parameters, cytokines, and demographics was determined using Pearson correlation coefficients. Means of the two groups were compared using the two-group t-test. Patients with IC/BPS had reduced monocyte oxygen consumption rates and glycolytic rates compared to healthy subjects. In contrast, lymphocytes from these patients had increased oxygen consumption rates and glycolytic rates. Several cytokines and chemokines including Interferon-gamma (IFN-ɣ), tumor necrosis factor alpha (TNF-ɑ), Interleukin-6 (IL-6), Interleukin-8 (IL-8) and vascular endothelial growth factor (VEGF) levels were significantly elevated in the plasma of patients with IC/BPS. However, Transforming growth factor (TGF-β) and Interleukin-10 (IL-10) levels were significantly decreased in IC/BPS patients compared to HS. In addition, Interferon gamma (IFN-ɣ), TNF-ɑ, IL-8, and TGF-β levels correlated with several bioenergetic parameters in monocytes or lymphocytes from healthy subjects. In contrast, TNF-ɑ and IL-8 correlated with bioenergetic parameters in monocytes from IC/BPS patients. Monocyte and lymphocyte cellular bioenergetics and plasma cytokine levels are different in patients with IC/PBS compared to HS. It appears that systemic inflammation is greater in this cohort which may negatively impact immune cell function. The relationship between cellular bioenergetics and inflammation in monocytes and lymphocytes could be important in understanding the pathogenesis of IC/PBS and warrants further investigation.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Monocyte mitochondrial respiration and glycolysis in healthy subjects and patients with Interstitial Cystitis/Bladder Pain Syndrome (IC/BPS).
Distribution of (A) basal, (B) ATP-linked, (C) Proton Leak, (D) Maximal, (E) Reserve Capacity, and (F) Non-mitochondrial OCR parameters as well as (G) Basal ECAR and (H) Oligo-sensitive ECAR parameters in monocytes from study participants. Data expressed as mean ± SD, n = 5–6 replicates; up to n  = 17 HS, n = 16 IC/BPS. *p<0.05, different from HS.
Fig 2
Fig 2. Lymphocyte mitochondrial respiration and glycolysis in healthy subjects and patients with Interstitial Cystitis/Bladder Pain Syndrome (IC/BPS).
Distribution of (A) basal, (B) ATP-linked, (C) Proton Leak, (D) Maximal, (E) Reserve Capacity, and (F) Non-mitochondrial OCR parameters as well as (G) Basal ECAR and (H) Oligo-sensitive ECAR parameters in lymphocytes from study participants. Data expressed as mean ± SD, n = 5–6 replicates; up to n  = 16 HS, n = 13 IC/BPS. *p<0.05, ***p<0.001 different from HS.
Fig 3
Fig 3. Plasma pro-inflammatory cytokine levels in healthy subjects (HS) and patients with Interstitial Cystitis/Bladder Pain Syndrome (IC/BPS).
Distribution of plasma (A) IFN-ɣ (B) TNF-ɑ, (C) TGF-β, (D) IL-6, (E) IL-8, (F) IL-10, (G) VEGF, (H) IL-23/23 p40, and (I) GM-CSF levels in study participants; Results are presented as mean ± SD; up to n  = 15 HS, n = 16 IC/BPS *p<0.05 compared to HS.
Fig 4
Fig 4. Correlation heat map between mitochondrial metabolic responses and cytokine levels in monocytes and lymphocytes from healthy subjects (HS) and patients with Interstitial Cystitis/Bladder Pain Syndrome (IC/BPS).
The parametric correlation coefficients of (A) monocyte or (B) lymphocyte maximal respiration/reserve capacity oxygen consumption rates vs various plasma cytokine levels are shown. Red shades represent positive correlations and blue shades represent negative correlations. Data are from n = 18 HS and n = 18 IC/BPS.
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