Bacterial Lipopolysaccharides Exacerbate Neurogenic Heterotopic Ossification Development.
ANIMAL MODELS
CYTOKINES
DISEASES AND DISORDERS OF/RELATED TO BONE (OTHER)
OSTEOIMMUNOLOGY
Journal
Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research
ISSN: 1523-4681
Titre abrégé: J Bone Miner Res
Pays: United States
ID NLM: 8610640
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
24
07
2023
received:
07
03
2023
accepted:
15
08
2023
medline:
4
12
2023
pubmed:
21
8
2023
entrez:
21
8
2023
Statut:
ppublish
Résumé
Neurogenic heterotopic ossifications (NHO) are heterotopic bones that develop in periarticular muscles after severe central nervous system (CNS) injuries. Several retrospective studies have shown that NHO prevalence is higher in patients who suffer concomitant infections. However, it is unclear whether these infections directly contribute to NHO development or reflect the immunodepression observed in patients with CNS injury. Using our mouse model of NHO induced by spinal cord injury (SCI) between vertebrae T
Substances chimiques
Lipopolysaccharides
0
Minerals
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1700-1717Subventions
Organisme : Collège Français des Enseignants Universitaires de Médecine Physique et de Réadaptation
Organisme : Direction Générale de l'Armement DGA
Organisme : Mater Foundation
Organisme : National Health and Medical Research Council
Organisme : U.S. Department of Defense
Organisme : University of Queensland
Informations de copyright
© 2023 The Authors. Journal of Bone and Mineral Research published by Wiley Periodicals LLC on behalf of American Society for Bone and Mineral Research (ASBMR).
Références
Genet F, Jourdan C, Schnitzler A, et al. Troublesome heterotopic ossification after central nervous system damage: a survey of 570 surgeries. PLoS One. 2011;6(1):e16632.
van Kuijk AA, Geurts AC, van Kuppevelt HJ. Neurogenic heterotopic ossification in spinal cord injury. Spinal Cord. 2002;40(7):313-326.
Dizdar D, Tiftik T, Kara M, et al. Risk factors for developing heterotopic ossification in patients with traumatic brain injury. Brain Inj. 2013;27(7-8):807-811.
Reznik JE, Biros E, Marshall R, et al. Prevalence and risk-factors of neurogenic heterotopic ossification in traumatic spinal cord and traumatic brain injured patients admitted to specialised units in Australia. J Musculoskelet Neuronal Interact. 2014;14(1):19-28.
Garland DE, Orwin JF. Resection of heterotopic ossification in patients with spinal cord injuries. Clin Orthop Relat Res. 1989;242:169-176.
Vanden Bossche L, Vanderstraeten G. Heterotopic ossification: a review. J Rehabil Med. 2005;37(3):129-136.
Genet F, Chehensse C, Jourdan C, et al. Impact of the operative delay and the degree of neurologic sequelae on recurrence of excised heterotopic ossification in patients with traumatic brain injury. J Head Trauma Rehabil. 2012;27(6):443-448.
Genet F, Marmorat JL, Lautridou C, et al. Impact of late surgical intervention on heterotopic ossification of the hip after traumatic neurological injury. J Bone Jt Surg Br. 2009;91(11):1493-1498.
Genêt F, Minooee K, Jourdan C, et al. Troublesome heterotopic ossification and stroke: features and risk factors. A case control study. Brain Inj. 2018;29(7-8):866-871.
Ohlmeier M, Suero EM, Aach M, et al. Muscle localization of heterotopic ossification following spinal cord injury. Spine J. 2017;17(10):1519-1522.
Almangour W, Schnitzler A, Salga M, et al. Recurrence of heterotopic ossification after removal in patients with traumatic brain injury: a systematic review. Ann Phys Rehabil Med. 2016;59(4):263-269.
Alexander KA, Tseng H-W, Salga M, Genêt F, Levesque J-P. When the nervous system turns skeletal muscles into bones: how to solve the conundrum of neurogenic heterotopic ossification. Curr Osteoporos Rep. 2020;18(6):666-676.
Hendricks HT, Geurts AC, van Ginneken BC, Heeren AJ, Vos PE. Brain injury severity and autonomic dysregulation accurately predict heterotopic ossification in patients with traumatic brain injury. Clin Rehabil. 2007;21(6):545-553.
Citak M, Suero EM, Backhaus M, et al. Risk factors for heterotopic ossification in patients with spinal cord injury: a case-control study of 264 patients. Spine. 2012;37(23):1953-1957.
van Kampen PJ, Martina JD, Vos PE, Hoedemaekers CW, Hendricks HT. Potential risk factors for developing heterotopic ossification in patients with severe traumatic brain injury. J Head Trauma Rehabil. 2011;26(5):384-391.
Suero EM, Meindl R, Schildhauer TA, Citak M. Clinical prediction rule for heterotopic ossification of the hip in patients with spinal cord injury. Spine. 2018;43(22):1572-1578.
Genêt F, Kulina I, Vaquette C, et al. Neurological heterotopic ossification following spinal cord injury is triggered by macrophage-mediated inflammation in muscle. J Pathol. 2015;236(2):229-240.
Debaud C, Tseng H-W, Chedik M, et al. Local and systemic factors drive ectopic osteogenesis in regenerating muscles of spinal cord-injured mice in a lesion level-dependent manner. J Neurotrauma. 2021;38(15):2162-2175.
Tseng H-W, Girard D, Alexander KA, et al. Spinal cord injury reprograms muscle fibroadipogenic progenitors to form heterotopic bones within muscles. Bone Res. 2022;10(1):22.
Alexander KA, Tseng H-W, Kulina I, et al. Lymphocytes are not required for neurogenic heterotopic ossification development after spinal cord injury. Neurotrauma Rep. 2022;3(1):87-96.
Tseng H-W, Kulina I, Salga M, et al. Neurogenic heterotopic ossifications develop independently of granulocyte colony-stimulating factor and neutrophils. J Bone Miner Res. 2020;35(11):2242-2251.
Tseng H-W, Kulina I, Girard D, et al. Interleukin-1 is overexpressed in injured muscles following spinal cord injury and promotes neurogenic heterotopic ossification. J Bone Miner Res. 2022;37(3):531-546.
Torossian F, Guerton B, Anginot A, et al. Macrophage-derived oncostatin M contributes to human and mouse neurogenic heterotopic ossifications. JCI Insight. 2017;2(21):e96034.
Alexander KA, Tseng H-W, Fleming W, et al. Inhibition of JAK1/2 tyrosine kinases reduces neurogenic heterotopic ossification after spinal cord injury. Front Immunol. 2019;10:377.
Dinarello CA, Simon A, van der Meer JWM. Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nat Rev Drug Discovery. 2012;11(8):633-652.
Gong Y, Yan X, Sun X, et al. Oncostatin M is a prognostic biomarker and inflammatory mediator for sepsis. J Infect Dis. 2020;221(12):1989-1998.
Salim SY, AlMalki N, Macala KF, et al. Oncostatin M receptor type II knockout mitigates inflammation and improves survival from sepsis in mice. Biomedicine. 2023;11(2):483.
Hoshino K, Takeuchi O, Kawai T, et al. Toll-like receptor 4 (Tlr4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for Tlr4 as the Lps gene product. J Immunol. 1999;162(7):3749-3752.
Adachi O, Kawai T, Takeda K, et al. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity. 1998;9(1):143-150.
Yamamoto M, Sato S, Hemmi H, et al. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science. 2003;301(5633):640-643.
Lilley E, Andrews MR, Bradbury EJ, et al. Refining rodent models of spinal cord injury. Exp Neurol. 2020;328:113273.
Kitajima S, Takuma S, Morimoto M. Histological analysis of murine colitis induced by dextran sulfate sodium of different molecular weights. Exp Anim. 2000;49(1):9-15.
Perse M, Cerar A. Dextran sodium sulphate colitis mouse model: traps and tricks. J Biomed Biotechnol. 2012;2012:718617.
Erben U, Loddenkemper C, Doerfel K, et al. A guide to histomorphological evaluation of intestinal inflammation in mouse models. Int J Clin Exp Pathol. 2014;7(8):4557-4576.
Breslow N. Design and analysis of case-control studies. Annu Rev Public Health. 1982;3:29-54.
Seymour CW, Liu VX, Iwashyna TJ, et al. Assessment of clinical criteria for sepsis: for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA. 2016;315(8):762-774.
Shankar-Hari M, Phillips GS, Levy ML, et al. Developing a new definition and assessing new clinical criteria for septic shock: for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA. 2016;315(8):775-787.
Baker SP, O'Neill B, Haddon W Jr, Long WB. The injury severity score: a method for describing patients with multiple injuries and evaluating emergency care. J Trauma. 1974;14(3):187-196.
Vincent JL, Sakr Y, Sprung CL, et al. Sepsis in European intensive care units: results of the SOAP study. Crit Care Med. 2006;34(2):344-353.
Vincent J-L, Rello J, Marshall J, et al. International study of the prevalence and outcomes of infection in intensive care units. JAMA. 2009;302(21):2323-2329.
Le Gall JR, Lemeshow S, Saulnier F. A new simplified acute physiology score (SAPS II) based on a European/North American multicenter study. JAMA. 1993;270(24):2957-2963.
Fink MP. Animal models of sepsis. Virulence. 2014;5(1):143-153.
Tateda K, Matsumoto T, Miyazaki S, Yamaguchi K. Lipopolysaccharide-induced lethality and cytokine production in aged mice. Infect Immun. 1996;64(3):769-774.
Nagai Y, Akashi S, Nagafuku M, et al. Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat Immunol. 2002;3(7):667-672.
Shibata T, Motoi Y, Tanimura N, et al. Intracellular TLR4/MD-2 in macrophages senses gram-negative bacteria and induces a unique set of LPS-dependent genes. Int Immunol. 2011;23(8):503-510.
Zeuner M, Bieback K, Widera D. Controversial role of toll-like receptor 4 in adult stem cells. Stem Cell Rev Rep. 2015;11(4):621-634.
Sambasivan R, Yao R, Kissenpfennig A, et al. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development. 2011;138(17):3647-3656.
Moncrieffe MC, Bollschweiler D, Li B, et al. Myd88 death-domain oligomerization determines myddosome architecture: implications for toll-like receptor signaling. Structure. 2020;28(3):281-289.e3.
Bryant CE, Symmons M, Gay NJ. Toll-like receptor signalling through macromolecular protein complexes. Mol Immunol. 2015;63(2):162-165.
Kigerl KA, Hall JCE, Wang L, et al. Gut dysbiosis impairs recovery after spinal cord injury. J Exp Med. 2016;213(12):2603-2620.
Yan Y, Kolachala V, Dalmasso G, et al. Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. PLoS One. 2009;4(6):e6073.
Madaro L, Passafaro M, Sala D, et al. Denervation-activated STAT3-IL-6 signalling in fibro-adipogenic progenitors promotes myofibres atrophy and fibrosis. Nat Cell Biol. 2018;20(8):917-927.
Meisel C, Schwab JM, Prass K, Meisel A, Dirnagl U. Central nervous system injury-induced immune deficiency syndrome. Nat Rev Neurosci. 2005;6(10):775-786.
Held KS, Lane TE. Spinal cord injury, immunodepression, and antigenic challenge. Semin Immunol. 2014;26(5):415-420.
Zhang Y, Guan Z, Reader B, et al. Autonomic dysreflexia causes chronic immune suppression after spinal cord injury. J Neurosci. 2013;33(32):12970-12981.
Jung W-C, Levesque J-P, Ruitenberg MJ. It takes nerve to fight back: the significance of neural innervation of the bone marrow and spleen for immune function. Semin Cell Dev Biol. 2017;61:60-70.
Hindi SM, Shin J, Gallot YS, et al. MyD88 promotes myoblast fusion in a cell-autonomous manner. Nat Commun. 2017;8(1):1624.
Pavey GJ, Qureshi AT, Hope DN, et al. Bioburden increases heterotopic ossification formation in an established rat model. Clin Orthop Relat Res. 2015;473(9):2840-2847.
Olmsted-Davis E, Mejia J, Salisbury E, Gugala Z, Davis AR. A population of M2 macrophages associated with bone formation. Front Immunol. 2021;12:686769.
Matsumoto A, Takami M, Urano E, et al. Lipopolysaccharide (LPS) inhibits ectopic bone formation induced by bone morphogenetic protein-2 and TGF-β1 through IL-1β production. J Oral Biosci. 2020;62(1):44-51.
Bott KN, Feldman E, de Souza RJ, et al. Lipopolysaccharide-induced bone loss in rodent models: a systematic review and meta-analysis. J Bone Miner Res. 2023;38(1):198-213.
Guo C, Yuan L, Wang JG, et al. Lipopolysaccharide (LPS) induces the apoptosis and inhibits osteoblast differentiation through JNK pathway in MC3T3-E1 cells. Inflammation. 2014;37(2):621-631.
Bandow K, Maeda A, Kakimoto K, et al. Molecular mechanisms of the inhibitory effect of lipopolysaccharide (LPS) on osteoblast differentiation. Biochem Biophys Res Commun. 2010;402(4):755-761.
Mo IF, Yip KH, Chan WK, et al. Prolonged exposure to bacterial toxins downregulated expression of toll-like receptors in mesenchymal stromal cell-derived osteoprogenitors. BMC Cell Biol. 2008;9:52.
van den Berk LC, Jansen BJ, Siebers-Vermeulen KG, et al. Toll-like receptor triggering in cord blood mesenchymal stem cells. J Cell Mol Med. 2009;13(9b):3415-3426.
Albiero ML, Amorim BR, Martins L, et al. Exposure of periodontal ligament progenitor cells to lipopolysaccharide from Escherichia coli changes osteoblast differentiation pattern. J Appl Oral Sci. 2015;23(2):145-152.
He X, Wang H, Jin T, et al. TLR4 activation promotes bone marrow MSC proliferation and osteogenic differentiation via Wnt3a and Wnt5a signaling. PLoS One. 2016;11(3):e0149876.
Sacchetti B, Funari A, Remoli C, et al. No identical "mesenchymal stem cells" at different times and sites: human committed progenitors of distinct origin and differentiation potential are incorporated as adventitial cells in microvessels. Stem Cell Rep. 2016;6(6):897-913.
Valido E, Bertolo A, Fränkl GP, et al. Systematic review of the changes in the microbiome following spinal cord injury: animal and human evidence. Spinal Cord. 2022;60(4):288-300.
Jogia T, Ruitenberg MJ. Traumatic spinal cord injury and the gut microbiota: current insights and future challenges. Front Immunol. 2020;11:704.
Nayfach S, Shi ZJ, Seshadri R, Pollard KS, Kyrpides NC. New insights from uncultivated genomes of the global human gut microbiome. Nature. 2019;568(7753):505-510.
Thefenne L, de Brier G, Leclerc T, et al. Two new risk factors for heterotopic ossification development after severe burns. PLoS One. 2017;12(8):e0182303.
Orchard GR, Paratz JD, Blot S, Roberts JA. Risk factors in hospitalized patients with burn injuries for developing heterotopic ossification-a retrospective analysis. J Burn Care Res. 2015;36(4):465-470.
Evans KN, Forsberg JA, Potter BK, et al. Inflammatory cytokine and chemokine expression is associated with heterotopic ossification in high-energy penetrating war injuries. J Orthop Trauma. 2012;26(11):e204-e213.
Manrique J, Alijanipour P, Heller S, Dove M, Parvizi J. Increased risk of heterotopic ossification following revision hip arthroplasty for periprosthetic joint infection. Arch Bone Jt Surg. 2018;6(6):486-491.
Rosteius T, Rausch V, Pätzholz S, et al. Incidence and risk factors for heterotopic ossification following periprosthetic joint infection of the hip. Arch Orthop Trauma Surg. 2019;139(9):1307-1314.
Scott BN, Roberts DJ, Robertson HL, et al. Incidence, prevalence, and occurrence rate of infection among adults hospitalized after traumatic brain injury: study protocol for a systematic review and meta-analysis. Syst Rev. 2013;2:68.
Helling TS, Evans LL, Fowler DL, Hays LV, Kennedy FR. Infectious complications in patients with severe head injury. J Trauma. 1988;28(11):1575-1577.
Garcia-Arguello LY, O'Horo JC, Farrell A, et al. Infections in the spinal cord-injured population: a systematic review. Spinal Cord. 2017;55(6):526-534.
Ferrucci JL, Sassi FC, Medeiros GC, Andrade CRF. Comparison between the functional aspects of swallowing and clinical markers in ICU patients with traumatic brain injury (TBI). CoDAS. 2019;31(2):e20170278.
Nakata H, Yamakawa K, Kabata D, et al. Identifying septic shock populations benefitting from polymyxin B hemoperfusion: a prospective cohort study incorporating a restricted cubic spline regression model. Shock. 2020;54(5):667-674.
Opal SM, Laterre P-F, Francois B, et al. Effect of eritoran, an antagonist of MD2-TLR4, on mortality in patients with severe sepsis: the ACCESS randomized trial. JAMA. 2013;309(11):1154-1162.
Rice TW, Wheeler AP, Bernard GR, et al. A randomized, double-blind, placebo-controlled trial of TAK-242 for the treatment of severe sepsis. Crit Care Med. 2010;38(8):1685-1694.