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Article ; Online: The role of the complement system in disc degeneration and Modic changes.

Heggli, Irina / Teixeira, Graciosa Q / Iatridis, James C / Neidlinger-Wilke, Cornelia / Dudli, Stefan

JOR spine

2024 Volume 7, Issue 1, Page(s) e1312

Abstract: Disc degeneration and vertebral endplate bone marrow lesions called Modic changes are prevalent spinal pathologies found in chronic low back pain patients. Their pathomechanisms are complex and not fully understood. Recent studies have revealed that ... ...

Abstract	Disc degeneration and vertebral endplate bone marrow lesions called Modic changes are prevalent spinal pathologies found in chronic low back pain patients. Their pathomechanisms are complex and not fully understood. Recent studies have revealed that complement system proteins and interactors are dysregulated in disc degeneration and Modic changes. The complement system is part of the innate immune system and plays a critical role in tissue homeostasis. However, its dysregulation has also been associated with various pathological conditions such as rheumatoid arthritis and osteoarthritis. Here, we review the evidence for the involvement of the complement system in intervertebral disc degeneration and Modic changes. We found that only a handful of studies reported on complement factors in Modic changes and disc degeneration. Therefore, the level of evidence for the involvement of the complement system is currently low. Nevertheless, the complement system is tightly intertwined with processes known to occur during disc degeneration and Modic changes, such as increased cell death, autoantibody production, bacterial defense processes, neutrophil activation, and osteoclast formation, indicating a contribution of the complement system to these spinal pathologies. Based on these mechanisms, we propose a model how the complement system could contribute to the vicious cycle of tissue damage and chronic inflammation in disc degeneration and Modic changes. With this review, we aim to highlight a currently understudied but potentially important inflammatory pathomechanism of disc degeneration and Modic changes that may be a novel therapeutic target.
Language	English
Publishing date	2024-02-02
Publishing country	United States
Document type	Journal Article ; Review
ISSN	2572-1143
ISSN (online)	2572-1143
DOI	10.1002/jsp2.1312
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Article ; Online: Impacts of priming on distinct immunosuppressive mechanisms of mesenchymal stromal cells under translationally relevant conditions.

Herger, Nick / Heggli, Irina / Mengis, Tamara / Devan, Jan / Arpesella, Leonardo / Brunner, Florian / Distler, Oliver / Dudli, Stefan

Stem cell research & therapy

2024 Volume 15, Issue 1, Page(s) 65

Abstract: Background: The multimodal properties of mesenchymal stromal cells (MSCs), particularly their ability to modulate immune responses is of high interest in translational research. Pro-inflammatory, hypoxic, and 3D culture priming are promising and often ... ...

Abstract	Background: The multimodal properties of mesenchymal stromal cells (MSCs), particularly their ability to modulate immune responses is of high interest in translational research. Pro-inflammatory, hypoxic, and 3D culture priming are promising and often used strategies to improve the immunosuppressive potency of MSCs, but the underlying mechanisms are not well understood. Therefore, the aims of this study were (i) to compare the effects of pro-inflammatory, hypoxic, and 3D culture priming on the in vitro immunosuppressive potential of MSCs, (ii) to assess if immunosuppressive priming effects are temporally preserved under standard and translationally relevant culture conditions, and (iii) to investigate if the three priming strategies engage the same immunosuppressive mechanisms. Methods: Functional in vitro T cell suppressive potency measurements were conducted to assess the impact of pro-inflammatory, hypoxic, and 3D culture priming on the immunosuppressive potential of human bone marrow-derived MSCs. Primed MSCs were either cultured under standard cell culture conditions or translationally relevant culture conditions, and their transcriptomic adaptations were monitored over time. Next-generation sequencing was performed to assess if different priming strategies activate distinct immunosuppressive mechanisms. Results: (i) Pro-inflammatory, hypoxic, and 3D culture priming induced profound transcriptomic changes in MSCs resulting in a significantly enhanced T cell suppressive potential of pro-inflammatory and 3D culture primed MSCs. (ii) Priming effects rapidly faded under standard cell culture conditions but were partially preserved under translationally relevant conditions. Interestingly, continuous 3D culture priming of MSCs maintained the immunosuppressive potency of MSCs. (iii) Next-generation sequencing revealed that priming strategy-specific differentially expressed genes are involved in the T cell suppressive capacity of MSCs, indicating that different priming strategies engage distinct immunosuppressive mechanisms. Conclusion: Priming can be a useful approach to improve the immunosuppressive potency of MSCs. However, future studies involving primed MSCs should carefully consider the significant impact of translationally relevant conditions on the preservation of priming effects. Continuous 3D culture could act as a functionalized formulation, supporting the administration of MSC spheroids for a sustainably improved immunosuppressive potency.
MeSH term(s)	Humans ; Mesenchymal Stem Cells ; Cell Culture Techniques ; Gene Expression Profiling ; High-Throughput Nucleotide Sequencing ; Hypoxia ; Immunosuppressive Agents
Chemical Substances	Immunosuppressive Agents
Language	English
Publishing date	2024-03-05
Publishing country	England
Document type	Journal Article
ZDB-ID	2548671-8
ISSN	1757-6512 ; 1757-6512
ISSN (online)	1757-6512
ISSN	1757-6512
DOI	10.1186/s13287-024-03677-5
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Article ; Online: Intervertebral disc microbiome in Modic changes: Lack of result replication underscores the need for a consensus in low-biomass microbiome analysis.

Mengis, Tamara / Zajac, Natalia / Bernhard, Laura / Heggli, Irina / Herger, Nick / Devan, Jan / Marcus, Roy / Brunner, Florian / Laux, Christoph / Farshad, Mazda / Distler, Oliver / Dudli, Stefan

JOR spine

2024 Volume 7, Issue 2, Page(s) e1330

Abstract: Introduction: The emerging field of the disc microbiome challenges traditional views of disc sterility, which opens new avenues for novel clinical insights. However, the lack of methodological consensus in disc microbiome studies introduces ... ...

Abstract	Introduction: The emerging field of the disc microbiome challenges traditional views of disc sterility, which opens new avenues for novel clinical insights. However, the lack of methodological consensus in disc microbiome studies introduces discrepancies. The aims of this study were to (1) compare the disc microbiome of non-Modic (nonMC), Modic type 1 change (MC1), and MC2 discs to findings from prior disc microbiome studies, and (2) investigate if discrepancies to prior studies can be explained with bioinformatic variations. Methods: Sequencing of 16S rRNA in 70 discs (24 nonMC, 25 MC1, and 21 MC2) for microbiome profiling. The experimental setup included buffer contamination controls and was performed under aseptic conditions. Methodology and results were contrasted with previous disc microbiome studies. Critical bioinformatic steps that were different in our best-practice approach and previous disc microbiome studies (taxonomic lineage assignment, prevalence cut-off) were varied and their effect on results were compared. Results: There was limited overlap of results with a previous study on MC disc microbiome. No bacterial genera were shared using the same bioinformatic parameters. Taxonomic lineage assignment using "amplicon sequencing variants" was more sensitive and detected 48 genera compared to 22 with "operational taxonomic units" (previous study). Increasing filter cut-off from 4% to 50% (previous study) reduced genera from 48 to 4 genera. Despite these differences, both studies observed dysbiosis with an increased abundance of gram-negative bacteria in MC discs as well as a lower beta-diversity. Conclusion: There is dysbiosis in MC discs. Bioinformatic parameters impact results yet cannot explain the different findings from this and a previous study. Therefore, discrepancies are likely caused by different sample preparations or true biologic differences. Harmonized protocols are required to advance understanding of the disc microbiome and its clinical implications.
Language	English
Publishing date	2024-04-04
Publishing country	United States
Document type	Journal Article
ISSN	2572-1143
ISSN (online)	2572-1143
DOI	10.1002/jsp2.1330
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Article: Bone marrow stromal cells in Modic type 1 changes promote neurite outgrowth.

Mengis, Tamara / Herger, Nick / Heggli, Irina / Devan, Jan / Spirig, José Miguel / Laux, Christoph J / Brunner, Florian / Farshad, Mazda / Distler, Oliver / Dudli, Stefan

Frontiers in cell and developmental biology

2023 Volume 11, Page(s) 1286280

Abstract: The pain in patients with Modic type 1 changes (MC1) is often due to vertebral body endplate pain, which is linked to abnormal neurite outgrowth in the vertebral body and adjacent endplate. The aim of this study was to understand the role of MC1 bone ... ...

Abstract	The pain in patients with Modic type 1 changes (MC1) is often due to vertebral body endplate pain, which is linked to abnormal neurite outgrowth in the vertebral body and adjacent endplate. The aim of this study was to understand the role of MC1 bone marrow stromal cells (BMSCs) in neurite outgrowth. BMSCs can produce neurotrophic factors, which have been shown to be pro-fibrotic in MC1, and expand in the perivascular space where sensory vertebral nerves are located. The study involved the exploration of the BMSC transcriptome in MC1, co-culture of MC1 BMSCs with the neuroblastoma cell line SH-SY5Y, analysis of supernatant cytokines, and analysis of gene expression changes in co-cultured SH-SY5Y. Transcriptomic analysis revealed upregulated brain-derived neurotrophic factor (BDNF) signaling-related pathways. Co-cultures of MC1 BMSCs with SH-SY5Y cells resulted in increased neurite sprouting compared to co-cultures with control BMSCs. The concentration of BDNF and other cytokines supporting neuron growth was increased in MC1 vs. control BMSC co-culture supernatants. Taken together, these findings show that MC1 BMSCs provide strong pro-neurotrophic cues to nearby neurons and could be a relevant disease-modifying treatment target.
Language	English
Publishing date	2023-10-25
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2737824-X
ISSN	2296-634X
ISSN	2296-634X
DOI	10.3389/fcell.2023.1286280
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Article ; Online: Acute and chronic effects of a light-activated FGF receptor in keratinocytes in vitro and in mice.

Rauschendorfer, Theresa / Gurri, Selina / Heggli, Irina / Maddaluno, Luigi / Meyer, Michael / Inglés-Prieto, Álvaro / Janovjak, Harald / Werner, Sabine

Life science alliance

2021 Volume 4, Issue 11

Abstract: FGFs and their high-affinity receptors (FGFRs) play key roles in development, tissue repair, and disease. Because FGFRs bind overlapping sets of ligands, their individual functions cannot be determined using ligand stimulation. Here, we generated a light- ...

Abstract	FGFs and their high-affinity receptors (FGFRs) play key roles in development, tissue repair, and disease. Because FGFRs bind overlapping sets of ligands, their individual functions cannot be determined using ligand stimulation. Here, we generated a light-activated FGFR2 variant (OptoR2) to selectively activate signaling by the major FGFR in keratinocytes. Illumination of OptoR2-expressing HEK 293T cells activated FGFR signaling with remarkable temporal precision and promoted cell migration and proliferation. In murine and human keratinocytes, OptoR2 activation rapidly induced the classical FGFR signaling pathways and expression of FGF target genes. Surprisingly, multi-level counter-regulation occurred in keratinocytes in vitro and in transgenic mice in vivo, including OptoR2 down-regulation and loss of responsiveness to light activation. These results demonstrate unexpected cell type-specific limitations of optogenetic FGFRs in long-term in vitro and in vivo settings and highlight the complex consequences of transferring optogenetic cell signaling tools into their relevant cellular contexts.
MeSH term(s)	Animals ; Female ; Fibroblast Growth Factors/metabolism ; Fibroblast Growth Factors/physiology ; HEK293 Cells ; Humans ; Keratinocytes/metabolism ; Keratinocytes/physiology ; Ligands ; Light ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Receptor, Fibroblast Growth Factor, Type 2/genetics ; Receptor, Fibroblast Growth Factor, Type 2/metabolism ; Receptors, Fibroblast Growth Factor/genetics ; Receptors, Fibroblast Growth Factor/metabolism ; Receptors, Fibroblast Growth Factor/physiology ; Signal Transduction
Chemical Substances	Ligands ; Receptors, Fibroblast Growth Factor ; Fibroblast Growth Factors (62031-54-3) ; Receptor, Fibroblast Growth Factor, Type 2 (EC 2.7.10.1)
Language	English
Publishing date	2021-09-21
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	2575-1077
ISSN (online)	2575-1077
DOI	10.26508/lsa.202101100
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Article ; Online: Extrinsic Macrophages Protect While Tendon Progenitors Degrade: Insights from a Tissue Engineered Model of Tendon Compartmental Crosstalk.

Stauber, Tino / Wolleb, Maja / Duss, Anja / Jaeger, Patrick K / Heggli, Irina / Hussien, Amro A / Blache, Ulrich / Snedeker, Jess G

Advanced healthcare materials

2021 Volume 10, Issue 20, Page(s) e2100741

Abstract: Tendons are among the most mechanically stressed tissues of the body, with a functional core of type-I collagen fibers maintained by embedded stromal fibroblasts known as tenocytes. The intrinsic load-bearing core compartment of tendon is surrounded, ... ...

Abstract	Tendons are among the most mechanically stressed tissues of the body, with a functional core of type-I collagen fibers maintained by embedded stromal fibroblasts known as tenocytes. The intrinsic load-bearing core compartment of tendon is surrounded, nourished, and repaired by the extrinsic peritendon, a synovial-like tissue compartment with access to tendon stem/progenitor cells as well as blood monocytes. In vitro tendon model systems generally lack this important feature of tissue compartmentalization, while in vivo models are cumbersome when isolating multicellular mechanisms. To bridge this gap, an improved in vitro model of explanted tendon core stromal tissue (mouse tail tendon fascicles) surrounded by cell-laden collagen hydrogels that mimic extrinsic tissue compartments is suggested. Using this model, CD146
MeSH term(s)	Animals ; Collagen ; Macrophages ; Mice ; Tendon Injuries ; Tendons ; Tenocytes
Chemical Substances	Collagen (9007-34-5)
Language	English
Publishing date	2021-09-08
Publishing country	Germany
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2649576-4
ISSN	2192-2659 ; 2192-2640
ISSN (online)	2192-2659
ISSN	2192-2640
DOI	10.1002/adhm.202100741
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Article ; Online: Intervertebral disc cell chondroptosis elicits neutrophil response in

Schweizer, Tiziano A / Andreoni, Federica / Acevedo, Claudio / Scheier, Thomas C / Heggli, Irina / Maggio, Ewerton Marques / Eberhard, Nadia / Brugger, Silvio D / Dudli, Stefan / Zinkernagel, Annelies S

Frontiers in immunology

2022 Volume 13, Page(s) 908211

Abstract: To understand the pathophysiology of spondylodiscitis due ... ...

Abstract	To understand the pathophysiology of spondylodiscitis due to
MeSH term(s)	Animals ; Cytokines/metabolism ; Discitis/metabolism ; Discitis/pathology ; Humans ; Intervertebral Disc/metabolism ; Neutrophils/metabolism ; Retrospective Studies ; Staphylococcal Infections/metabolism ; Staphylococcus aureus/metabolism ; Swine
Chemical Substances	Cytokines
Language	English
Publishing date	2022-07-28
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.908211
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Article ; Online: CD90-positive stromal cells associate with inflammatory and fibrotic changes in modic changes.

Dudli, Stefan / Karol, Agnieszka / Giudici, Luca / Heggli, Irina / Laux, Christoph J / Spirig, Jose M / Wanivenhaus, Florian / Betz, Michael / Germann, Christoph / Farshad-Amacker, Nadja / Brunner, Florian / Distler, Oliver / Farshad, Mazda

Osteoarthritis and cartilage open

2022 Volume 4, Issue 3, Page(s) 100287

Abstract: Objective: Modic changes (MC) are vertebral bone marrow lesions seen on magnetic resonance images, that associate with disc degeneration and low back pain (LBP). Few studies described MC histopathology qualitatively based on a few patient samples. CD90- ... ...

Abstract	Objective: Modic changes (MC) are vertebral bone marrow lesions seen on magnetic resonance images, that associate with disc degeneration and low back pain (LBP). Few studies described MC histopathology qualitatively based on a few patient samples. CD90-positive bone marrow stromal cells were shown to be pro-fibrotic in MC. We aimed to provide the first semi-quantitative histomorphometric analysis of MC bone marrow. We hypothesized a role of CD90-positive cells in MC pathomechanisms. Design: Human biopsies from Modic type 1 changes (MC1, n = 8), Modic type 2 changes (MC2, n = 6), and control biopsies (MC0, n = 8) from adjacent vertebrae were obtained from 14 LBP patients during lumbar spinal fusion. Biopsies were processed for histology/immunohistochemistry. Inflammatory changes (oedema, inflammatory infiltrates), fibrotic changes (connective tissue, type I and III collagen, fibronectin, α-smooth muscle actin), and amount of bone marrow stromal cells (CD90, CD105) were scored. Scores for MC0, MC1, and MC2 were compared with non-parametric tests. Pairwise correlations, hierarchical clustering, and principal component analysis of histological readouts were calculated to identify most important histomorphometric MC characteristics. Results: Compared to MC0, MC1 had more connective tissue, oedema, inflammatory infiltrates, and CD90 Conclusion: Accumulation of CD90
Language	English
Publishing date	2022-06-22
Publishing country	England
Document type	Journal Article
ISSN	2665-9131
ISSN (online)	2665-9131
DOI	10.1016/j.ocarto.2022.100287
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Article ; Online: Role of C-reactive protein in the bone marrow of Modic type 1 changes.

Dudli, Stefan / Heggli, Irina / Laux, Christoph J / Spirig, José M / Wanivenhaus, Florian / Betz, Michael / Germann, Christoph / Farshad-Amacker, Nadja A / Herger, Nick / Mengis, Tamara / Brunner, Florian / Farshad, Mazda / Distler, Oliver

Journal of orthopaedic research : official publication of the Orthopaedic Research Society

2022 Volume 41, Issue 5, Page(s) 1115–1122

Abstract: Modic type 1 changes (MC1) are vertebral bone marrow lesions and associate with low back pain. Increased serum C-reactive protein (CRP) has inconsistently been associated with MC1. We aimed to provide evidence for the role of CRP in the tissue ... ...

Abstract	Modic type 1 changes (MC1) are vertebral bone marrow lesions and associate with low back pain. Increased serum C-reactive protein (CRP) has inconsistently been associated with MC1. We aimed to provide evidence for the role of CRP in the tissue pathophysiology of MC1 bone marrow. From 13 MC1 patients undergoing spinal fusion at MC1 levels, vertebral bone marrow aspirates from MC1 and intrapatient control bone marrow were taken. Bone marrow CRP, interleukin (IL)-1, and IL-6 were measured with enzyme-linked immunosorbent assays; lactate dehydrogenase (LDH) was measured with a colorimetric assay. CRP, IL-1, and IL-6 were compared between MC1 and control bone marrow. Bone marrow CRP was correlated with blood CRP and with bone marrow IL-1, IL-6, and LDH. CRP expression by marrow cells was measured with a polymerase chain reaction. Increased CRP in MC1 bone marrow (mean difference: +0.22 mg CRP/g, 95% confidence interval [CI] [-0.04, 0.47], p = 0.088) correlated with blood CRP (r = 0.69, p = 0.018), with bone marrow IL-1β (ρ = 0.52, p = 0.029) and IL-6 (ρ = 0.51, p = 0.031). Marrow cells did not express CRP. Increased LDH in MC1 bone marrow (143.1%, 95% CI [110.7%, 175.4%], p = 0.014) indicated necrosis. A blood CRP threshold of 3.2 mg/L detected with 100% accuracy increased CRP in MC1 bone marrow. In conclusion, the association of CRP with inflammatory and necrotic changes in MC1 bone marrow provides evidence for a pathophysiological role of CRP in MC1 bone marrow.
MeSH term(s)	Humans ; C-Reactive Protein/metabolism ; Bone Marrow/pathology ; Interleukin-6 ; Low Back Pain/pathology
Chemical Substances	C-Reactive Protein (9007-41-4) ; Interleukin-6
Language	English
Publishing date	2022-09-14
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	605542-4
ISSN	1554-527X ; 0736-0266
ISSN (online)	1554-527X
ISSN	0736-0266
DOI	10.1002/jor.25437
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Zs.A 1879: Show issues

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Article ; Online: Modic type 2 changes are fibroinflammatory changes with complement system involvement adjacent to degenerated vertebral endplates.

Heggli, Irina / Laux, Christoph J / Mengis, Tamara / Karol, Agnieszka / Cornaz, Frédéric / Herger, Nick / Aradi-Vegh, Borbala / Widmer, Jonas / Burkhard, Marco D / Farshad-Amacker, Nadja A / Pfammatter, Sibylle / Wolski, Witold E / Brunner, Florian / Distler, Oliver / Farshad, Mazda / Dudli, Stefan

JOR spine

2022 Volume 6, Issue 1, Page(s) e1237

Abstract: Background: Vertebral endplate signal intensity changes visualized by magnetic resonance imaging termed Modic changes (MC) are highly prevalent in low back pain patients. Interconvertibility between the three MC subtypes (MC1, MC2, MC3) suggests ... ...

Abstract	Background: Vertebral endplate signal intensity changes visualized by magnetic resonance imaging termed Modic changes (MC) are highly prevalent in low back pain patients. Interconvertibility between the three MC subtypes (MC1, MC2, MC3) suggests different pathological stages. Histologically, granulation tissue, fibrosis, and bone marrow edema are signs of inflammation in MC1 and MC2. However, different inflammatory infiltrates and amount of fatty marrow suggest distinct inflammatory processes in MC2. Aims: The aims of this study were to investigate (i) the degree of bony (BEP) and cartilage endplate (CEP) degeneration in MC2, (ii) to identify inflammatory MC2 pathomechanisms, and (iii) to show that these marrow changes correlate with severity of endplate degeneration. Methods: Pairs of axial biopsies ( Results: Endplates from MC2 were significantly more degenerated. Proteomic analysis revealed an activated complement system, increased expression of extracellular matrix proteins, angiogenic, and neurogenic factors in MC2 marrow. Endplate scores correlated with upregulated complement and neurogenic proteins. Discussion: The inflammatory pathomechanisms in MC2 comprises activation of the complement system. Concurrent inflammation, fibrosis, angiogenesis, and neurogenesis indicate that MC2 is a chronic inflammation. Correlation of endplate damage with complement and neurogenic proteins suggest that complement system activation and neoinnervation may be linked to endplate damage. The endplate-near marrow is the pathomechanistic site, because MC2 occur at locations with more endplate degeneration. Conclusion: MC2 are fibroinflammatory changes with complement system involvement which occur adjacent to damaged endplates.
Language	English
Publishing date	2022-12-23
Publishing country	United States
Document type	Journal Article
ISSN	2572-1143
ISSN (online)	2572-1143
DOI	10.1002/jsp2.1237
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