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Erschienen in: Pediatric Surgery International 11/2022

22.08.2022 | Original Article

Intrauterine exposure to oxidative stress induces caspase-1-dependent enteric nerve cell pyroptosis

verfasst von: Lingling Zhou, Bingyu Wang, Hua Xie, Chunxia Du, Jie Tang, Weibing Tang

Erschienen in: Pediatric Surgery International | Ausgabe 11/2022

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Abstract

Purpose

This study determined whether oxidative stress causes the developmental abnormalities of the enteric nervous system during the embryonic period.

Methods

Using the test results of tissue specimens of children with Hirschsprung disease (HSCR), we established a pregnant rat model of oxidative stress and a cellular oxidative stress model to conduct related molecular, cellular, and histopathological experiments for exploration and validation.

Results

The results of the quantitative real-time polymerase chain reaction assay indicated overexpression of pyroptosis markers (NLRP3, ASC, and caspase-1) in HSCR lesions and newborn pups in the oxidative stress group (treated with d-galactose). The expression of cathepsin D was significantly decreased in intestinal tissues of newborn pups in the oxidative stress group compared to the control group. Reactive oxygen species scavengers (N-acetyl-cysteine, NAC), the caspase-1 inhibitor (VX-765), and the NLRP3 siRNA could reverse the release of LDH, decrease the number of propidium iodide stained cells, and reduce the percentage of TUNEL/caspase-3 double-positive cells in the H2O2-treated group.

Conclusion

Oxidative stress can induce the death of enteric nerve cells by activating caspase-1-dependent pyroptosis through NLRP3 inflammasomes, which may contribute to abnormal enteric nervous system development.
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Literatur
1.
Zurück zum Zitat Furness JB, Callaghan BP, Rivera LR, Cho HJ (2014) The enteric nervous system and gastrointestinal innervation: integrated local and central control. Adv Exp Med Biol 817:39–71PubMedCrossRef Furness JB, Callaghan BP, Rivera LR, Cho HJ (2014) The enteric nervous system and gastrointestinal innervation: integrated local and central control. Adv Exp Med Biol 817:39–71PubMedCrossRef
2.
3.
Zurück zum Zitat Kapur RP (2000) Colonization of the murine hindgut by sacral crest-derived neural precursors: experimental support for an evolutionarily conserved model. Dev Biol 227:146–155PubMedCrossRef Kapur RP (2000) Colonization of the murine hindgut by sacral crest-derived neural precursors: experimental support for an evolutionarily conserved model. Dev Biol 227:146–155PubMedCrossRef
4.
Zurück zum Zitat Heuckeroth RO (2018) Hirschsprung disease—integrating basic science and clinical medicine to improve outcomes. Nat Rev Gastroenterol Hepatol 15:152–167PubMedCrossRef Heuckeroth RO (2018) Hirschsprung disease—integrating basic science and clinical medicine to improve outcomes. Nat Rev Gastroenterol Hepatol 15:152–167PubMedCrossRef
5.
Zurück zum Zitat Goldstein AM, Cox NJ (2019) Complex simplicity and Hirschsprung’s disease. N Engl J Med 380:1478–1479PubMedCrossRef Goldstein AM, Cox NJ (2019) Complex simplicity and Hirschsprung’s disease. N Engl J Med 380:1478–1479PubMedCrossRef
6.
Zurück zum Zitat Chatterjee S, Nandakumar P, Auer DR, Gabriel SB, Chakravarti A (2019) Gene- and tissue-level interactions in normal gastrointestinal development and Hirschsprung disease. Proc Natl Acad Sci USA 116:26697–26708PubMedCentralCrossRef Chatterjee S, Nandakumar P, Auer DR, Gabriel SB, Chakravarti A (2019) Gene- and tissue-level interactions in normal gastrointestinal development and Hirschsprung disease. Proc Natl Acad Sci USA 116:26697–26708PubMedCentralCrossRef
7.
Zurück zum Zitat Jaroy EG, Acosta-Jimenez L, Hotta R, Goldstein AM, Emblem R, Klungland A, Ougland R (2019) “Too much guts and not enough brains”: (epi)genetic mechanisms and future therapies of Hirschsprung disease—a review. Clin Epigenetics 11:135PubMedPubMedCentralCrossRef Jaroy EG, Acosta-Jimenez L, Hotta R, Goldstein AM, Emblem R, Klungland A, Ougland R (2019) “Too much guts and not enough brains”: (epi)genetic mechanisms and future therapies of Hirschsprung disease—a review. Clin Epigenetics 11:135PubMedPubMedCentralCrossRef
8.
Zurück zum Zitat Lake JI, Heuckeroth RO (2013) Enteric nervous system development: migration, differentiation, and disease. Am J Physiol Gastrointest Liver Physiol 305:G1-24PubMedPubMedCentralCrossRef Lake JI, Heuckeroth RO (2013) Enteric nervous system development: migration, differentiation, and disease. Am J Physiol Gastrointest Liver Physiol 305:G1-24PubMedPubMedCentralCrossRef
9.
Zurück zum Zitat Butler Tjaden NE, Trainor PA (2013) The developmental etiology and pathogenesis of Hirschsprung disease. Transl Res 162:1–15PubMedCrossRef Butler Tjaden NE, Trainor PA (2013) The developmental etiology and pathogenesis of Hirschsprung disease. Transl Res 162:1–15PubMedCrossRef
10.
Zurück zum Zitat Akbareian SE, Nagy N, Steiger CE, Mably JD, Miller SA, Hotta R, Molnar D, Goldstein AM (2013) Enteric neural crest-derived cells promote their migration by modifying their microenvironment through tenascin-C production. Dev Biol 382:446–456PubMedPubMedCentralCrossRef Akbareian SE, Nagy N, Steiger CE, Mably JD, Miller SA, Hotta R, Molnar D, Goldstein AM (2013) Enteric neural crest-derived cells promote their migration by modifying their microenvironment through tenascin-C production. Dev Biol 382:446–456PubMedPubMedCentralCrossRef
11.
Zurück zum Zitat Nakazawa N, Miyahara K, Okawada M, Yamataka A, Suzuki R, Akazawa C, Tomikawa-Ichikawa N, Arikawa-Hirasawa E (2013) Laminin-1 promotes enteric nervous system development in mouse embryo. Pediatr Surg Int 29:1205–1208PubMedCrossRef Nakazawa N, Miyahara K, Okawada M, Yamataka A, Suzuki R, Akazawa C, Tomikawa-Ichikawa N, Arikawa-Hirasawa E (2013) Laminin-1 promotes enteric nervous system development in mouse embryo. Pediatr Surg Int 29:1205–1208PubMedCrossRef
12.
13.
Zurück zum Zitat Nagy N, Guyer RA, Hotta R, Zhang D, Newgreen DF, Halasy V, Kovacs T, Goldstein AM (2020) RET overactivation leads to concurrent Hirschsprung disease and intestinal ganglioneuromas. Development 147:dev190900PubMedPubMedCentralCrossRef Nagy N, Guyer RA, Hotta R, Zhang D, Newgreen DF, Halasy V, Kovacs T, Goldstein AM (2020) RET overactivation leads to concurrent Hirschsprung disease and intestinal ganglioneuromas. Development 147:dev190900PubMedPubMedCentralCrossRef
14.
Zurück zum Zitat Wen Z, Shen Q, Zhang H, Su Y, Zhu Z, Chen G, Peng L, Li H, Du C, Xie H, Xu X, Tang W (2019) Circular RNA CCDC66 targets DCX to regulate cell proliferation and migration by sponging miR-488-3p in Hirschsprung’s disease. J Cell Physiol 234:10576–10587PubMedCrossRef Wen Z, Shen Q, Zhang H, Su Y, Zhu Z, Chen G, Peng L, Li H, Du C, Xie H, Xu X, Tang W (2019) Circular RNA CCDC66 targets DCX to regulate cell proliferation and migration by sponging miR-488-3p in Hirschsprung’s disease. J Cell Physiol 234:10576–10587PubMedCrossRef
15.
Zurück zum Zitat Su Y, Wen Z, Shen Q, Zhang H, Peng L, Chen G, Zhu Z, Du C, Xie H, Li H, Xia Y, Tang W (2018) Long non-coding RNA LOC100507600 functions as a competitive endogenous RNA to regulate BMI1 expression by sponging miR128–1–3p in Hirschsprung’s disease. Cell Cycle 17:1–9CrossRef Su Y, Wen Z, Shen Q, Zhang H, Peng L, Chen G, Zhu Z, Du C, Xie H, Li H, Xia Y, Tang W (2018) Long non-coding RNA LOC100507600 functions as a competitive endogenous RNA to regulate BMI1 expression by sponging miR128–1–3p in Hirschsprung’s disease. Cell Cycle 17:1–9CrossRef
16.
Zurück zum Zitat Hameister R, Kaur C, Dheen ST, Lohmann CH, Singh G (2020) Reactive oxygen/nitrogen species (ROS/RNS) and oxidative stress in arthroplasty. J Biomed Mater Res B Appl Biomater 108:2073–2087PubMedCrossRef Hameister R, Kaur C, Dheen ST, Lohmann CH, Singh G (2020) Reactive oxygen/nitrogen species (ROS/RNS) and oxidative stress in arthroplasty. J Biomed Mater Res B Appl Biomater 108:2073–2087PubMedCrossRef
17.
Zurück zum Zitat Fussell JC, Kelly FJ (2019) Oxidative contribution of air pollution to extrinsic skin ageing. Free Radic Biol Med 151:111–122PubMedCrossRef Fussell JC, Kelly FJ (2019) Oxidative contribution of air pollution to extrinsic skin ageing. Free Radic Biol Med 151:111–122PubMedCrossRef
18.
Zurück zum Zitat Kato M, Iwashita T, Takeda K, Akhand AA, Liu W, Yoshihara M, Asai N, Suzuki H, Takahashi M, Nakashima I (2000) Ultraviolet light induces redox reaction-mediated dimerization and superactivation of oncogenic ret tyrosine kinases. Mol Biol Cell 11:93–101PubMedPubMedCentralCrossRef Kato M, Iwashita T, Takeda K, Akhand AA, Liu W, Yoshihara M, Asai N, Suzuki H, Takahashi M, Nakashima I (2000) Ultraviolet light induces redox reaction-mediated dimerization and superactivation of oncogenic ret tyrosine kinases. Mol Biol Cell 11:93–101PubMedPubMedCentralCrossRef
21.
Zurück zum Zitat Mullen L, Mengozzi M, Hanschmann EM, Alberts B, Ghezzi P (2019) How the redox state regulates immunity. Free Radic Biol Med 157:3–14PubMedCrossRef Mullen L, Mengozzi M, Hanschmann EM, Alberts B, Ghezzi P (2019) How the redox state regulates immunity. Free Radic Biol Med 157:3–14PubMedCrossRef
22.
Zurück zum Zitat Kramer ER, Aron L, Ramakers GM, Seitz S, Zhuang X, Beyer K, Smidt MP, Klein R (2007) Absence of Ret signaling in mice causes progressive and late degeneration of the nigrostriatal system. PLoS Biol 5:e39PubMedPubMedCentralCrossRef Kramer ER, Aron L, Ramakers GM, Seitz S, Zhuang X, Beyer K, Smidt MP, Klein R (2007) Absence of Ret signaling in mice causes progressive and late degeneration of the nigrostriatal system. PLoS Biol 5:e39PubMedPubMedCentralCrossRef
23.
Zurück zum Zitat Kato M, Ninomiya H, Maeda M, Tanaka N, Ilmiawati C, Yoshinaga M (2016) Commentary to Gorelenkova Miller and Mieyal (2015): sulfhydryl-mediated redox signaling in inflammation: role in neurodegenerative diseases. Arch Toxicol 90:1017–1018PubMedCrossRef Kato M, Ninomiya H, Maeda M, Tanaka N, Ilmiawati C, Yoshinaga M (2016) Commentary to Gorelenkova Miller and Mieyal (2015): sulfhydryl-mediated redox signaling in inflammation: role in neurodegenerative diseases. Arch Toxicol 90:1017–1018PubMedCrossRef
24.
Zurück zum Zitat Hossain K, Akhand AA, Kato M, Du J, Takeda K, Wu J, Takeuchi K, Liu W, Suzuki H, Nakashima I (2000) Arsenite induces apoptosis of murine T lymphocytes through membrane raft-linked signaling for activation of c-Jun amino-terminal kinase. J Immunol 165:4290–4297PubMedCrossRef Hossain K, Akhand AA, Kato M, Du J, Takeda K, Wu J, Takeuchi K, Liu W, Suzuki H, Nakashima I (2000) Arsenite induces apoptosis of murine T lymphocytes through membrane raft-linked signaling for activation of c-Jun amino-terminal kinase. J Immunol 165:4290–4297PubMedCrossRef
25.
Zurück zum Zitat Guo YL, Chakraborty S, Rajan SS, Wang R, Huang F (2010) Effects of oxidative stress on mouse embryonic stem cell proliferation, apoptosis, senescence, and self-renewal. Stem Cells Dev 19:1321–1331PubMedPubMedCentralCrossRef Guo YL, Chakraborty S, Rajan SS, Wang R, Huang F (2010) Effects of oxidative stress on mouse embryonic stem cell proliferation, apoptosis, senescence, and self-renewal. Stem Cells Dev 19:1321–1331PubMedPubMedCentralCrossRef
26.
Zurück zum Zitat Cho KA, Suh JW, Lee KH, Kang JL, Woo SY (2012) IL-17 and IL-22 enhance skin inflammation by stimulating the secretion of IL-1beta by keratinocytes via the ROS-NLRP3-caspase-1 pathway. Int Immunol 24:147–158PubMedCrossRef Cho KA, Suh JW, Lee KH, Kang JL, Woo SY (2012) IL-17 and IL-22 enhance skin inflammation by stimulating the secretion of IL-1beta by keratinocytes via the ROS-NLRP3-caspase-1 pathway. Int Immunol 24:147–158PubMedCrossRef
27.
Zurück zum Zitat Xue Y, Enosi Tuipulotu D, Tan WH, Kay C, Man SM (2019) Emerging activators and regulators of inflammasomes and pyroptosis. Trends Immunol 40:1035–1052PubMedCrossRef Xue Y, Enosi Tuipulotu D, Tan WH, Kay C, Man SM (2019) Emerging activators and regulators of inflammasomes and pyroptosis. Trends Immunol 40:1035–1052PubMedCrossRef
28.
Zurück zum Zitat Shi J, Gao W, Shao F (2017) Pyroptosis: gasdermin-mediated programmed necrotic cell death. Trends Biochem Sci 42:245–254PubMedCrossRef Shi J, Gao W, Shao F (2017) Pyroptosis: gasdermin-mediated programmed necrotic cell death. Trends Biochem Sci 42:245–254PubMedCrossRef
29.
Zurück zum Zitat Winkler S, Rosen-Wolff A (2015) Caspase-1: an integral regulator of innate immunity. Seminars in immunopathology 37:419–427PubMedCrossRef Winkler S, Rosen-Wolff A (2015) Caspase-1: an integral regulator of innate immunity. Seminars in immunopathology 37:419–427PubMedCrossRef
31.
Zurück zum Zitat Gulbransen BD, Bashashati M, Hirota SA, Gui X, Roberts JA, MacDonald JA, Muruve DA, McKay DM, Beck PL, Mawe GM, Thompson RJ, Sharkey KA (2012) Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat Med 18:600–604PubMedPubMedCentralCrossRef Gulbransen BD, Bashashati M, Hirota SA, Gui X, Roberts JA, MacDonald JA, Muruve DA, McKay DM, Beck PL, Mawe GM, Thompson RJ, Sharkey KA (2012) Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat Med 18:600–604PubMedPubMedCentralCrossRef
32.
Zurück zum Zitat Fann DY, Lee SY, Manzanero S, Chunduri P, Sobey CG, Arumugam TV (2013) Pathogenesis of acute stroke and the role of inflammasomes. Ageing Res Rev 12:941–966PubMedCrossRef Fann DY, Lee SY, Manzanero S, Chunduri P, Sobey CG, Arumugam TV (2013) Pathogenesis of acute stroke and the role of inflammasomes. Ageing Res Rev 12:941–966PubMedCrossRef
33.
Zurück zum Zitat Ishrat T, Mohamed IN, Pillai B, Soliman S, Fouda AY, Ergul A, El-Remessy AB, Fagan SC (2015) Thioredoxin-interacting protein: a novel target for neuroprotection in experimental thromboembolic stroke in mice. Mol Neurobiol 51:766–778PubMedCrossRef Ishrat T, Mohamed IN, Pillai B, Soliman S, Fouda AY, Ergul A, El-Remessy AB, Fagan SC (2015) Thioredoxin-interacting protein: a novel target for neuroprotection in experimental thromboembolic stroke in mice. Mol Neurobiol 51:766–778PubMedCrossRef
34.
Zurück zum Zitat Crowley LC, Marfell BJ, Waterhouse NJ (2016) Detection of DNA fragmentation in apoptotic cells by TUNEL. Cold Spring Harb Protoc 2016:pdb-prot087221CrossRef Crowley LC, Marfell BJ, Waterhouse NJ (2016) Detection of DNA fragmentation in apoptotic cells by TUNEL. Cold Spring Harb Protoc 2016:pdb-prot087221CrossRef
35.
Zurück zum Zitat Abu-Alfa AK, Kuan SF, West AB, Reyes-Múgica M (1997) Cathepsin D in intestinal ganglion cells. A potential aid to diagnosis in suspected Hirschsprung’s disease. Am J Surg Pathol 21:201–205PubMedCrossRef Abu-Alfa AK, Kuan SF, West AB, Reyes-Múgica M (1997) Cathepsin D in intestinal ganglion cells. A potential aid to diagnosis in suspected Hirschsprung’s disease. Am J Surg Pathol 21:201–205PubMedCrossRef
36.
Zurück zum Zitat Karaca G, Karaca ZM, Kayhan B, Bayindir Y, Kayabas U, Toplu S, Elmasdag S, Onalan E, Yesilada E (2019) The relationship between caspase-1 related inflammasome expression and serum inflammatory cytokine levels during acute brucellosis. North Clin Istanb 6:117–123PubMed Karaca G, Karaca ZM, Kayhan B, Bayindir Y, Kayabas U, Toplu S, Elmasdag S, Onalan E, Yesilada E (2019) The relationship between caspase-1 related inflammasome expression and serum inflammatory cytokine levels during acute brucellosis. North Clin Istanb 6:117–123PubMed
38.
Zurück zum Zitat Wang Y, Jiang Q, Cai H, Xu Z, Wu W, Gu B, Li L, Cai W (2020) Genetic variants in RET, ARHGEF3 and CTNNAL1, and relevant interaction networks, contribute to the risk of Hirschsprung disease. Aging (Albany NY). 12:4379PubMedPubMedCentralCrossRef Wang Y, Jiang Q, Cai H, Xu Z, Wu W, Gu B, Li L, Cai W (2020) Genetic variants in RET, ARHGEF3 and CTNNAL1, and relevant interaction networks, contribute to the risk of Hirschsprung disease. Aging (Albany NY). 12:4379PubMedPubMedCentralCrossRef
39.
Zurück zum Zitat Heanue TA, Pachnis V (2007) Enteric nervous system development and Hirschsprung’s disease: advances in genetic and stem cell studies. Nat Rev Neurosci 8:466–479PubMedCrossRef Heanue TA, Pachnis V (2007) Enteric nervous system development and Hirschsprung’s disease: advances in genetic and stem cell studies. Nat Rev Neurosci 8:466–479PubMedCrossRef
40.
Zurück zum Zitat Lotfollahzadeh S, Taherian M, Anand S (2020) Hirschsprung disease. StatPearls, Treasure Island Lotfollahzadeh S, Taherian M, Anand S (2020) Hirschsprung disease. StatPearls, Treasure Island
41.
Zurück zum Zitat Jiang Q, Arnold S, Heanue T, Kilambi KP, Doan B, Kapoor A, Ling AY, Sosa MX, Guy M, Jiang Q, Burzynski G, West K, Bessling S, Griseri P, Amiel J, Fernandez RM, Verheij JB, Hofstra RM, Borrego S, Lyonnet S, Ceccherini I, Gray JJ, Pachnis V, McCallion AS, Chakravarti A (2015) Functional loss of semaphorin 3C and/or semaphorin 3D and their epistatic interaction with ret are critical to Hirschsprung disease liability. Am J Hum Genet 96:581–596PubMedPubMedCentralCrossRef Jiang Q, Arnold S, Heanue T, Kilambi KP, Doan B, Kapoor A, Ling AY, Sosa MX, Guy M, Jiang Q, Burzynski G, West K, Bessling S, Griseri P, Amiel J, Fernandez RM, Verheij JB, Hofstra RM, Borrego S, Lyonnet S, Ceccherini I, Gray JJ, Pachnis V, McCallion AS, Chakravarti A (2015) Functional loss of semaphorin 3C and/or semaphorin 3D and their epistatic interaction with ret are critical to Hirschsprung disease liability. Am J Hum Genet 96:581–596PubMedPubMedCentralCrossRef
42.
Zurück zum Zitat Ye L, Li G, Goebel A, Raju AV, Kong F, Lv Y, Li K, Zhu Y, Raja S, He P, Li F, Mwangi SM, Hu W, Srinivasan S (2020) Caspase-11-mediated enteric neuronal pyroptosis underlies Western diet-induced colonic dysmotility. J Clin Investig 130:3621–3636PubMedPubMedCentralCrossRef Ye L, Li G, Goebel A, Raju AV, Kong F, Lv Y, Li K, Zhu Y, Raja S, He P, Li F, Mwangi SM, Hu W, Srinivasan S (2020) Caspase-11-mediated enteric neuronal pyroptosis underlies Western diet-induced colonic dysmotility. J Clin Investig 130:3621–3636PubMedPubMedCentralCrossRef
44.
Zurück zum Zitat Kuwar R, Rolfe A, Di L, Xu H, He L, Jiang Y, Zhang S, Sun D (2019) A novel small molecular NLRP3 inflammasome inhibitor alleviates neuroinflammatory response following traumatic brain injury. J Neuroinflammation 16:81PubMedPubMedCentralCrossRef Kuwar R, Rolfe A, Di L, Xu H, He L, Jiang Y, Zhang S, Sun D (2019) A novel small molecular NLRP3 inflammasome inhibitor alleviates neuroinflammatory response following traumatic brain injury. J Neuroinflammation 16:81PubMedPubMedCentralCrossRef
45.
Zurück zum Zitat Li H, Zhou L, Zhi Z, Lv X, Wei Z, Zhang X, Tang W, Tong M (2020) Lipopolysaccharide upregulates miR-132/212 in Hirschsprung-associated enterocolitis, facilitating pyroptosis by activating NLRP3 inflammasome via targeting Sirtuin 1 (SIRT1). Aging 12:18588–18602PubMedPubMedCentralCrossRef Li H, Zhou L, Zhi Z, Lv X, Wei Z, Zhang X, Tang W, Tong M (2020) Lipopolysaccharide upregulates miR-132/212 in Hirschsprung-associated enterocolitis, facilitating pyroptosis by activating NLRP3 inflammasome via targeting Sirtuin 1 (SIRT1). Aging 12:18588–18602PubMedPubMedCentralCrossRef
46.
Zurück zum Zitat Chen X, Liu G, Yuan Y, Wu G, Wang S, Yuan L (2019) NEK7 interacts with NLRP3 to modulate the pyroptosis in inflammatory bowel disease via NF-kappaB signaling. Cell Death Dis 10:906PubMedPubMedCentralCrossRef Chen X, Liu G, Yuan Y, Wu G, Wang S, Yuan L (2019) NEK7 interacts with NLRP3 to modulate the pyroptosis in inflammatory bowel disease via NF-kappaB signaling. Cell Death Dis 10:906PubMedPubMedCentralCrossRef
47.
Zurück zum Zitat Pastor AC, Osman F, Teitelbaum DH, Caty MG, Langer JC (2009) Development of a standardized definition for Hirschsprung’s-associated enterocolitis: a delphi analysis. J Pediatr Surg 44:251–256PubMedCrossRef Pastor AC, Osman F, Teitelbaum DH, Caty MG, Langer JC (2009) Development of a standardized definition for Hirschsprung’s-associated enterocolitis: a delphi analysis. J Pediatr Surg 44:251–256PubMedCrossRef
48.
49.
Zurück zum Zitat Ali SS, Ahsan H, Zia MK, Siddiqui T, Khan FH (2020) Understanding oxidants and antioxidants: classical team with new players. J Food Biochem 44:e13145PubMedCrossRef Ali SS, Ahsan H, Zia MK, Siddiqui T, Khan FH (2020) Understanding oxidants and antioxidants: classical team with new players. J Food Biochem 44:e13145PubMedCrossRef
50.
Zurück zum Zitat Yagami T, Yamamoto Y, Koma H (2019) Pathophysiological roles of intracellular proteases in neuronal development and neurological diseases. Mol Neurobiol 56:3090–3112PubMedCrossRef Yagami T, Yamamoto Y, Koma H (2019) Pathophysiological roles of intracellular proteases in neuronal development and neurological diseases. Mol Neurobiol 56:3090–3112PubMedCrossRef
51.
Zurück zum Zitat Bhatia S, Drake DM, Miller L, Wells PG (2019) Oxidative stress and DNA damage in the mechanism of fetal alcohol spectrum disorders. Birth Defects Res 111:714–748PubMedCrossRef Bhatia S, Drake DM, Miller L, Wells PG (2019) Oxidative stress and DNA damage in the mechanism of fetal alcohol spectrum disorders. Birth Defects Res 111:714–748PubMedCrossRef
52.
Zurück zum Zitat Aminzadeh M, Roghani M, Sarfallah A, Riazi GH (2018) TRPM2 dependence of ROS-induced NLRP3 activation in Alzheimer’s disease. Int Immunopharmacol 54:78–85PubMedCrossRef Aminzadeh M, Roghani M, Sarfallah A, Riazi GH (2018) TRPM2 dependence of ROS-induced NLRP3 activation in Alzheimer’s disease. Int Immunopharmacol 54:78–85PubMedCrossRef
53.
Zurück zum Zitat Ganjam GK, Bolte K, Matschke LA, Neitemeier S, Dolga AM, Hollerhage M, Hoglinger GU, Adamczyk A, Decher N, Oertel WH, Culmsee C (2019) Mitochondrial damage by alpha-synuclein causes cell death in human dopaminergic neurons. Cell Death Dis 10:865PubMedPubMedCentralCrossRef Ganjam GK, Bolte K, Matschke LA, Neitemeier S, Dolga AM, Hollerhage M, Hoglinger GU, Adamczyk A, Decher N, Oertel WH, Culmsee C (2019) Mitochondrial damage by alpha-synuclein causes cell death in human dopaminergic neurons. Cell Death Dis 10:865PubMedPubMedCentralCrossRef
54.
55.
Zurück zum Zitat Penn RB (2021) Honing in on the effectors of oxidative stress in the asthmatic lung: oxidised phosphatidylcholines. Eur Respir J 57:2003736PubMedCrossRef Penn RB (2021) Honing in on the effectors of oxidative stress in the asthmatic lung: oxidised phosphatidylcholines. Eur Respir J 57:2003736PubMedCrossRef
56.
Zurück zum Zitat Nakao A, Matsunaga Y, Hayashida K, Takahashi N (2021) Role of oxidative stress and Ca(2+) signaling in psychiatric disorders. Front Cell Dev Biol 9:615569PubMedPubMedCentralCrossRef Nakao A, Matsunaga Y, Hayashida K, Takahashi N (2021) Role of oxidative stress and Ca(2+) signaling in psychiatric disorders. Front Cell Dev Biol 9:615569PubMedPubMedCentralCrossRef
57.
Zurück zum Zitat Liu N, Lin MM, Huang SS, Liu ZQ, Wu JC, Liang ZQ, Qin ZH, Wang Y (2021) NADPH and mito-apocynin treatment protects against KA-induced excitotoxic injury through autophagy pathway. Front Cell Dev Biol 9:612554PubMedPubMedCentralCrossRef Liu N, Lin MM, Huang SS, Liu ZQ, Wu JC, Liang ZQ, Qin ZH, Wang Y (2021) NADPH and mito-apocynin treatment protects against KA-induced excitotoxic injury through autophagy pathway. Front Cell Dev Biol 9:612554PubMedPubMedCentralCrossRef
58.
Zurück zum Zitat Ricke KM, Pass T, Kimoloi S, Fahrmann K, Jungst C, Schauss A, Baris OR, Aradjanski M, Trifunovic A, Eriksson Faelker TM, Bergami M, Wiesner RJ (2020) Mitochondrial dysfunction combined with high calcium load leads to impaired antioxidant defense underlying the selective loss of nigral dopaminergic neurons. J Neurosci 40:1975–1986PubMedPubMedCentralCrossRef Ricke KM, Pass T, Kimoloi S, Fahrmann K, Jungst C, Schauss A, Baris OR, Aradjanski M, Trifunovic A, Eriksson Faelker TM, Bergami M, Wiesner RJ (2020) Mitochondrial dysfunction combined with high calcium load leads to impaired antioxidant defense underlying the selective loss of nigral dopaminergic neurons. J Neurosci 40:1975–1986PubMedPubMedCentralCrossRef
59.
Zurück zum Zitat Parajuli B, Sonobe Y, Horiuchi H, Takeuchi H, Mizuno T, Suzumura A (2013) Oligomeric amyloid beta induces IL-1beta processing via production of ROS: implication in Alzheimer’s disease. Cell Death Dis 4:e975PubMedPubMedCentralCrossRef Parajuli B, Sonobe Y, Horiuchi H, Takeuchi H, Mizuno T, Suzumura A (2013) Oligomeric amyloid beta induces IL-1beta processing via production of ROS: implication in Alzheimer’s disease. Cell Death Dis 4:e975PubMedPubMedCentralCrossRef
60.
Zurück zum Zitat Elsas LJ (2001) Prenatal diagnosis of galactose-l-phosphate uridyltransferase (GALT)-deficient galactosemia. Prenat Diagn 21:302–303PubMedCrossRef Elsas LJ (2001) Prenatal diagnosis of galactose-l-phosphate uridyltransferase (GALT)-deficient galactosemia. Prenat Diagn 21:302–303PubMedCrossRef
61.
Zurück zum Zitat Gubbels CS, Land JA, Rubio-Gozalbo ME (2008) Fertility and impact of pregnancies on the mother and child in classic galactosemia. Obstet Gynecol Surv 63:334–343PubMedCrossRef Gubbels CS, Land JA, Rubio-Gozalbo ME (2008) Fertility and impact of pregnancies on the mother and child in classic galactosemia. Obstet Gynecol Surv 63:334–343PubMedCrossRef
62.
Zurück zum Zitat Yu F, Hao S, Zhao Y, Yang H, Fan XL, Yang J (2011) In utero and lactational beta-carotene supplementation attenuates d-galactose-induced hearing loss in newborn rats. Food Chem Toxicol 49:1697–1704PubMedCrossRef Yu F, Hao S, Zhao Y, Yang H, Fan XL, Yang J (2011) In utero and lactational beta-carotene supplementation attenuates d-galactose-induced hearing loss in newborn rats. Food Chem Toxicol 49:1697–1704PubMedCrossRef
Metadaten
Titel
Intrauterine exposure to oxidative stress induces caspase-1-dependent enteric nerve cell pyroptosis
verfasst von
Lingling Zhou
Bingyu Wang
Hua Xie
Chunxia Du
Jie Tang
Weibing Tang
Publikationsdatum
22.08.2022
Verlag
Springer Berlin Heidelberg
Erschienen in
Pediatric Surgery International / Ausgabe 11/2022
Print ISSN: 0179-0358
Elektronische ISSN: 1437-9813
DOI
https://doi.org/10.1007/s00383-022-05199-8

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Wer ihn je erlebt hat, wird ihn nicht vergessen: den Schmerz, den die beim Öffnen oder Schließen des Reißverschlusses am Hosenschlitz eingeklemmte Haut am Penis oder Skrotum verursacht. Eine neue Methode für rasche Abhilfe hat ein US-Team getestet.

Ähnliche Überlebensraten nach Reanimation während des Transports bzw. vor Ort

29.05.2024 Reanimation im Kindesalter Nachrichten

Laut einer Studie aus den USA und Kanada scheint es bei der Reanimation von Kindern außerhalb einer Klinik keinen Unterschied für das Überleben zu machen, ob die Wiederbelebungsmaßnahmen während des Transports in die Klinik stattfinden oder vor Ort ausgeführt werden. Jedoch gibt es dabei einige Einschränkungen und eine wichtige Ausnahme.

Alter der Mutter beeinflusst Risiko für kongenitale Anomalie

28.05.2024 Kinder- und Jugendgynäkologie Nachrichten

Welchen Einfluss das Alter ihrer Mutter auf das Risiko hat, dass Kinder mit nicht chromosomal bedingter Malformation zur Welt kommen, hat eine ungarische Studie untersucht. Sie zeigt: Nicht nur fortgeschrittenes Alter ist riskant.

Begünstigt Bettruhe der Mutter doch das fetale Wachstum?

Ob ungeborene Kinder, die kleiner als die meisten Gleichaltrigen sind, schneller wachsen, wenn die Mutter sich mehr ausruht, wird diskutiert. Die Ergebnisse einer US-Studie sprechen dafür.

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