nach oben

Erschienen in:

01.12.2023 | Original Article

High intestinal vascular permeability in a murine model for Hirschsprung’s disease: implications for postoperative Hirschsprung-associated enterocolitis

verfasst von: Kazuto Suda, Shunsuke Yamada, Katsumi Miyahara, Naho Fujiwara, Seitaro Kosaka, Kumpei Abe, Shogo Seo, Shinji Nakamura, Geoffrey J. Lane, Atsuyuki Yamataka

Erschienen in: Pediatric Surgery International | Ausgabe 1/2023

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Intestinal vascular permeability (VP) in a murine model for Hirschsprung’s disease (HD) and postoperative Hirschsprung-associated enterocolitis (HAEC) were investigated.

Methods

Intestinal VP was determined using a Miles assay using 1% Evans blue injected into a superficial temporal vein of newborn endothelin receptor-B KO HD model (KO) and syngeneic wild-type (WT) mice (n = 5, respectively). Extravasated Evans blue in normoganglionic ileum (Ng-I), normoganglionic proximal colon (Ng-PC) and aganglionic distal colon (Ag-DC) was quantified by absorbance at 620 nm. Quantitative polymerase chain reaction (qPCR) for Vascular Endothelial Growth Factor A (VEGF-A), VEGF-B, CDH5, SELE and CD31, and immunofluorescence for CD31 were performed.

Results

VP was significantly higher in Ng-I, Ng-PC, and Ag-DC from KO than WT (p < 0.01, p < 0.05, and p < 0.05, respectively). qPCR demonstrated upregulated VEGF-A in Ng-I and Ag-DC, VEGF-B in Ng-I, and SELE in Ng-I and Ng-PC (p < 0.05, p < 0.05, p < 0.05, p < 0.01 and p < 0.05, respectively), and downregulated CDH5 in Ng-I and Ng-PC from KO (p < 0.05, respectively). Expression of CD31 mRNA in Ng-I and Ag-DC from KO was significantly higher on qPCR (p < 0.05) but differences on immunofluorescence were not significant.

Conclusions

VP may be etiologic for postoperative HAEC throughout the intestinal tract even after excision of aganglionic bowel.

Miyano G, Takeda M, Koga H, Okawada M, Nakazawa-Tanaka N, Ishii J et al (2018) Hirschsprung’s disease in the laparoscopic transanal pull-through era: implications of age at surgery and technical aspects. Pediatr Surg Int 34(2):183–188CrossRefPubMed

Svetanoff WJ, Lopez JJ, Briggs KB, Fraser JA, Fraser JD, Oyetunji TA et al (2022) Management of Hirschsprung associated enterocolitis-How different are practice strategies? An international pediatric endosurgery group (IPEG) survey. J Pediatr Surg 57(6):1119–1126CrossRefPubMed

Pruitt LCC, Skarda DE, Rollins MD, Bucher BT (2020) Hirschsprung-associated enterocolitis in children treated at US children’s hospitals. J Pediatr Surg 55(3):535–540CrossRefPubMed

Yildiz HM, Carlson TL, Goldstein AM, Carrier RL (2015) Mucus barriers to microparticles and microbes are altered in Hirschsprung’s disease. Macromol Biosci 15(5):712–718CrossRefPubMedPubMedCentral

Schrenk S, Schuster A, Klotz M, Schleser F, Lake J, Heuckeroth RO et al (2015) Vascular and neural stem cells in the gut: do they need each other? Histochem Cell Biol 143(4):397–410CrossRefPubMed

Scaldaferri F, Vetrano S, Sans M, Arena V, Straface G, Stigliano E et al (2009) VEGF-A links angiogenesis and inflammation in inflammatory bowel disease pathogenesis. Gastroenterology 136(2):585–95.e5CrossRefPubMed

Yano K, Liaw PC, Mullington JM, Shih SC, Okada H, Bodyak N et al (2006) Vascular endothelial growth factor is an important determinant of sepsis morbidity and mortality. J Exp Med 203(6):1447–1458CrossRefPubMedPubMedCentral

Maruyama K, Kidoya H, Takemura N, Sugisawa E, Takeuchi O, Kondo T et al (2020) Zinc finger protein St18 protects against septic death by inhibiting VEGF-A from macrophages. Cell Rep 32(2):107906CrossRefPubMed

Heinolainen K, Karaman S, D’Amico G, Tammela T, Sormunen R, Eklund L et al (2017) VEGFR3 modulates vascular permeability by controlling VEGF/VEGFR2 signaling. Circ Res 120(9):1414–1425CrossRefPubMedPubMedCentral

10.

Su G, Feng T, Pei T, Yang F, Sun D, Yu H et al (2021) Autophagy modulates FSS-induced epithelial-mesenchymal transition in hepatocellular carcinoma cells. Mol Carcinog 60(9):607–619CrossRefPubMed

11.

Doi Y, Okada T, Matsumoto H, Ichihara M, Ishida T, Kiwada H (2010) Combination therapy of metronomic S-1 dosing with oxaliplatin-containing polyethylene glycol-coated liposome improves antitumor activity in a murine colorectal tumor model. Cancer Sci 101(11):2470–2475CrossRefPubMed

12.

Aggarwal A, Jain M, Frykman PK, Xu C, Mukherjee S, Muensterer OJ (2013) Multiphoton microscopy to identify and characterize the transition zone in a mouse model of Hirschsprung disease. J Pediatr Surg 48(6):1288–1293CrossRefPubMedPubMedCentral

13.

Gombash Lampe SE, Kaspar BK, Foust KD (2014) Intravenous injections in neonatal mice. J Vis Exp 93:e52037

14.

Fujiwara N, Nakazawa-Tanaka N, Miyahara K, Arikawa-Hirasawa E, Akazawa C, Yamataka A (2018) Altered expression of laminin alpha1 in aganglionic colon of endothelin receptor-B null mouse model of Hirschsprung’s disease. Pediatr Surg Int 34(2):137–141CrossRefPubMed

15.

Lee B, Shin H, Oh JE, Park J, Park M, Yang SC et al (2021) An autophagic deficit in the uterine vessel microenvironment provokes hyperpermeability through deregulated VEGFA, NOS1, and CTNNB1. Autophagy 17(7):1649–1666CrossRefPubMed

16.

De Niz M, Brás D, Ouarné M, Pedro M, Nascimento AM, Henao Misikova L et al (2021) Organotypic endothelial adhesion molecules are key for Trypanosoma brucei tropism and virulence. Cell Rep 36(12):109741CrossRefPubMedPubMedCentral

17.

Zhang R, Wang X, Ni L, Di X, Ma B, Niu S et al (2020) COVID-19: melatonin as a potential adjuvant treatment. Life Sci 250:117583CrossRefPubMedPubMedCentral

18.

Vassiliou AG, Kotanidou A, Dimopoulou I, Orfanos SE (2020) Endothelial damage in acute respiratory distress syndrome. Int J Mol Sci 21(22):1CrossRef

19.

Kellner M, Noonepalle S, Lu Q, Srivastava A, Zemskov E, Black SM (2017) ROS signaling in the pathogenesis of acute lung injury (ALI) and acute respiratory distress syndrome (ARDS). Adv Exp Med Biol 967:105–137CrossRefPubMedPubMedCentral

20.

Fujiwara N, Miyahara K, Nakazawa-Tanaka N, Akazawa C, Yamataka A (2016) Altered differentiation of enteric neural crest-derived cells from endothelin receptor-B null mouse model of Hirschsprung’s disease. Pediatr Surg Int 32(12):1095–1101CrossRefPubMed

21.

D’Orléans-Juste P, Labonté J, Bkaily G, Choufani S, Plante M, Honoré JC (2002) Function of the endothelin(B) receptor in cardiovascular physiology and pathophysiology. Pharmacol Ther 95(3):221–238CrossRefPubMed

22.

Carpenter T, Schomberg S, Steudel W, Ozimek J, Colvin K, Stenmark K et al (2003) Endothelin B receptor deficiency predisposes to pulmonary edema formation via increased lung vascular endothelial cell growth factor expression. Circ Res 93(5):456–463CrossRefPubMed

23.

Patibandla PK, Tyagi N, Dean WL, Tyagi SC, Roberts AM, Lominadze D (2009) Fibrinogen induces alterations of endothelial cell tight junction proteins. J Cell Physiol 221(1):195–203CrossRefPubMedPubMedCentral

24.

Saijo H, Tatsumi N, Arihiro S, Kato T, Okabe M, Tajiri H et al (2015) Microangiopathy triggers, and inducible nitric oxide synthase exacerbates dextran sulfate sodium-induced colitis. Lab Invest 95(7):728–748CrossRefPubMed

25.

Lu M, Fan X, Liao W, Li Y, Ma L, Yuan M et al (2021) Identification of significant genes as prognostic markers and potential tumor suppressors in lung adenocarcinoma via bioinformatical analysis. BMC Cancer 21(1):616CrossRefPubMedPubMedCentral

26.

Zhang L, Luo B, Dang YW, He RQ, Chen G, Peng ZG et al (2019) The clinical significance of endothelin receptor type B in hepatocellular carcinoma and its potential molecular mechanism. Exp Mol Pathol 107:141–157CrossRefPubMed

27.

Llinàs L, Peinado VI, Ramon Goñi J, Rabinovich R, Pizarro S, Rodriguez-Roisin R et al (2011) Similar gene expression profiles in smokers and patients with moderate COPD. Pulm Pharmacol Ther 24(1):32–41CrossRefPubMed

28.

Kusafuka T, Wang Y, Puri P (1997) Mutation analysis of the RET, the endothelin-B receptor, and the endothelin-3 genes in sporadic cases of Hirschsprung’s disease. J Pediatr Surg 32(3):501–504CrossRefPubMed

Titel: High intestinal vascular permeability in a murine model for Hirschsprung’s disease: implications for postoperative Hirschsprung-associated enterocolitis
verfasst von: Kazuto Suda
Shunsuke Yamada
Katsumi Miyahara
Naho Fujiwara
Seitaro Kosaka
Kumpei Abe
Shogo Seo
Shinji Nakamura
Geoffrey J. Lane
Atsuyuki Yamataka
Publikationsdatum: 01.12.2023
Verlag: Springer Berlin Heidelberg
Erschienen in: Pediatric Surgery International / Ausgabe 1/2023
Print ISSN: 0179-0358
Elektronische ISSN: 1437-9813
DOI: https://doi.org/10.1007/s00383-022-05308-7

Update Pädiatrie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

High intestinal vascular permeability in a murine model for Hirschsprung’s disease: implications for postoperative Hirschsprung-associated enterocolitis