Histochemical characterization of muscularis macrophage loss and disruption of a miR-93-5p–AHNAK neuro-immune axis in Hirschsprung’s disease

Agarwal V, Bell GW, Nam JW, Bartel DP (2015) Predicting effective microRNA target sites in mammalian mRNAs. Elife 4:e05005. https://doi.org/10.7554/eLife.05005

Article  PubMed  PubMed Central  Google Scholar 

Avetisyan M, Rood JE, Huerta Lopez S, Sengupta R, Wright-Jin E, Dougherty JD, Behrens EM, Heuckeroth RO (2018) Muscularis macrophage development in the absence of an enteric nervous system. Proc Natl Acad Sci USA 115:4696–4701. https://doi.org/10.1073/pnas.1802490115

Article  CAS  PubMed  PubMed Central  Google Scholar 

Becker L, Nguyen L, Gill J, Kulkarni S, Pasricha PJ, Habtezion A (2018) Age-dependent shift in macrophage polarisation causes inflammation-mediated degeneration of enteric nervous system. Gut 67:827–836. https://doi.org/10.1136/gutjnl-2016-312940

Article  CAS  PubMed  Google Scholar 

Cailotto C, Gomez-Pinilla PJ, Costes LM, van der Vliet J, Di Giovangiulio M, Némethova A, Matteoli G, Boeckxstaens GE (2014) Neuro-anatomical evidence indicating indirect modulation of macrophages by vagal efferents in the intestine but not in the spleen. PLoS ONE 9:e87785. https://doi.org/10.1371/journal.pone.0087785

Article  CAS  PubMed  PubMed Central  Google Scholar 

Cavone L, McCann T, Drake LK, Aguzzi EA, Oprişoreanu AM, Pedersen E, Sandi S, Selvarajah J, Tsarouchas TM, Wehner D, Keatinge M, Mysiak KS, Henderson BEP, Dobie R, Henderson NC, Becker T, Becker CG (2021) A unique macrophage subpopulation signals directly to progenitor cells to promote regenerative neurogenesis in the zebrafish spinal cord. Dev Cell 56:1617–1630. https://doi.org/10.1016/j.devcel.2021.04.031

Article  CAS  PubMed  Google Scholar 

De Schepper S, Verheijden S, Aguilera-Lizarraga J, Viola MF, Boesmans W, Stakenborg N, Voytyuk I, Schmidt I, Boeckx B, de Dierckx Casterlé I, Baekelandt V, Gonzalez Dominguez E, Mack M, Depoortere I, De Strooper B, Sprangers B, Himmelreich U, Soenen S, Guilliams M, Vanden Berghe P, Jones E, Lambrechts D, Boeckxstaens G (2018) Self-maintaining gut macrophages are essential for intestinal homeostasis. Cell 175:400–415. https://doi.org/10.1016/j.cell.2018.07.048

Article  CAS  PubMed  Google Scholar 

Ferenczi S, Mogor F, Takacs P, Kovacs T, Toth VE, Varga ZV, Kovács K, Lohinai Z, Vass KC, Nagy N, Dora D (2023) Depletion of muscularis macrophages ameliorates inflammation-driven dysmotility in murine colitis model. Sci Rep 13:22451. https://doi.org/10.1038/s41598-023-50059-7

Article  CAS  PubMed  PubMed Central  Google Scholar 

Froh M, Thurman RG, Wheeler MD (2002) Molecular evidence for a glycine-gated chloride channel in macrophages and leukocytes. Am J Physiol Gastrointest Liver Physiol 283:G856–G863. https://doi.org/10.1152/ajpgi.00503.2001

Article  CAS  PubMed  Google Scholar 

Gabanyi I, Muller PA, Feighery L, Oliveira TY, Costa-Pinto FA, Mucida D (2016) Neuro-immune interactions drive tissue programming in intestinal macrophages. Cell 164:378–391. https://doi.org/10.1016/j.cell.2015.12.023

Article  CAS  PubMed  PubMed Central  Google Scholar 

Heanue TA, Pachnis V (2007) Enteric nervous system development and Hirschsprung’s disease: advances in genetic and stem cell studies. Nat Rev Neurosci 8:466–479. https://doi.org/10.1038/nrn2137

Article  CAS  PubMed  Google Scholar 

Hohaus A, Person V, Behlke J, Schaper J, Morano I, Haase H (2002) The carboxyl-terminal region of AHNAK provides a link between cardiac L-type Ca2+ channels and the actin-based cytoskeleton. FASEB J 16:1205–1216. https://doi.org/10.1096/fj.01-0855com

Article  CAS  PubMed  Google Scholar 

Ji Y, Tam PK, Tang CS (2021) Roles of enteric neural stem cell niche and enteric nervous system development in Hirschsprung disease. Int J Mol Sci 22:9659. https://doi.org/10.3390/ijms22189659

Article  CAS  PubMed  PubMed Central  Google Scholar 

Juan CX, Mao Y, Cao Q, Chen Y, Zhou LB, Li S, Chen H, Chen JH, Zhou GP, Jin R (2021) Exosome-mediated pyroptosis of miR-93-TXNIP-NLRP3 leads to functional difference between M1 and M2 macrophages in sepsis-induced acute kidney injury. Cell Mol Med 25:4786–4799. https://doi.org/10.1111/jcmm.16449

Article  CAS  Google Scholar 

Li Y, Lv X, Chen H, Zhi Z, Wei Z, Wang B, Zhou L, Li H, Tang W (2021) Peptide derived from AHNAK inhibits cell migration and proliferation in Hirschsprung’s disease by targeting the ERK1/2 pathway. J Proteome Res 20:2308–2318. https://doi.org/10.1021/acs.jproteome.0c00811

Article  CAS  PubMed  Google Scholar 

Lim HJ, Kang DH, Lim JM, Kang DM, Seong JK, Kang SW, Bae YS (2013) Function of AHNAK protein in aortic smooth muscle cell migration through Rac activation. Cardiovasc Res 97:302–310. https://doi.org/10.1093/cvr/cvs311

Article  CAS  PubMed  Google Scholar 

Liu ZM, Yang XL, Jiang F, Pan YC, Zhang L (2020) Matrine involves in the progression of gastric cancer through inhibiting miR-93-5p and upregulating the expression of target gene AHNAK. Cell Biochem 121:2467–2477. https://doi.org/10.1002/jcb.29469

Article  CAS  Google Scholar 

Luzón-Toro B, Gui H, Ruiz-Ferrer M, Sze-Man Tang C, Fernández RM, Sham PC, Torroglosa A, Kwong-Hang Tam P, Espino-Paisán L, Cherny SS, Bleda M, Enguix-Riego MV, Dopazo J, Antiñolo G, García-Barceló MM, Borrego S (2015) Exome sequencing reveals a high genetic heterogeneity on familial Hirschsprung disease. Sci Rep 5:16473. https://doi.org/10.1038/srep16473

Article  CAS  PubMed  PubMed Central  Google Scholar 

Matheis F, Muller PA, Graves CL, Gabanyi I, Kerner ZJ, Costa-Borges D, Ahrends T, Rosenstiel P, Mucida D (2020) Adrenergic signaling in muscularis macrophages limits infection-induced neuronal loss. Cell 180:64-78.e16. https://doi.org/10.1016/j.cell.2019.12.002

Article  CAS  PubMed  PubMed Central  Google Scholar 

Matteoli G, Gomez-Pinilla PJ, Nemethova A, Di Giovangiulio M, Cailotto C, van Bree SH, Michel K, Tracey KJ, Schemann M, Boesmans W, Van den Berghe P, Boeckxstaens GE (2014) A distinct vagal anti-inflammatory pathway modulates intestinal muscularis resident macrophages independent of the spleen. Gut 63:938–948. https://doi.org/10.1136/gutjnl-2013-304676

Article  CAS  PubMed  Google Scholar 

McKeown SJ, Stamp L, Hao MM, Young HM (2013) Hirschsprung disease: a developmental disorder of the enteric nervous system. Wires Dev Biol 2:113–129. https://doi.org/10.1002/wdev.57

Article  CAS  Google Scholar 

Muller PA, Koscsó B, Rajani GM, Stevanovic K, Berres ML, Hashimoto D, Mortha A, Leboeuf M, Li XM, Mucida D, Stanley ER, Dahan S, Margolis KG, Gershon MD, Merad M, Bogunovic M (2014) Crosstalk between muscularis macrophages and enteric neurons regulates gastrointestinal motility. Cell 158:300–313. https://doi.org/10.1016/j.cell.2014.04.050

Article  CAS  PubMed  PubMed Central  Google Scholar 

Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, Gordon S, Hamilton JA, Ivashkiv LB, Lawrence T, Locati M, Mantovani A, Martinez FO, Mege JL, Mosser DM, Natoli G, Saeij JP, Schultze JL, Shirey KA, Sica A, Suttles J, Udalova I, van Ginderachter JA, Vogel SN, Wynn TA (2014) Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41:14–20. https://doi.org/10.1016/j.immuni.2014.06.008

Article  CAS  PubMed  PubMed Central  Google Scholar 

Neshatian L, Gibbons SJ, Farrugia G (2015) Macrophages in diabetic gastroparesis–the missing link? Neurogastroenterol Motil 27:7–18. https://doi.org/10.1111/nmo.12418

Article  CAS  PubMed  Google Scholar 

Pegtel DM, Gould SJ (2019) Exosomes. Annu Rev Biochem 88:487–514. https://doi.org/10.1146/annurev-biochem-013118-111902

Article  CAS  PubMed  Google Scholar 

Phillips RJ, Powley TL (2012) Macrophages associated with the intrinsic and extrinsic autonomic innervation of the rat gastrointestinal tract. Auton Neurosci Basic Clin 169:12–27. https://doi.org/10.1016/j.autneu.2012.02.004

Article  Google Scholar 

Prada I, Gabrielli M, Turola E, Iorio A, D’Arrigo G, Parolisi R, De Luca M, Pacifici M, Bastoni M, Lombardi M, Legname G, Cojoc D, Buffo A, Furlan R, Peruzzi F, Verderio C (2018) Glia-to-neuron transfer of miRNAs via extracellular vesicles: a new mechanism underlying inflammation-induced synaptic alterations. Acta Neuropathol 135:529–550. https://doi.org/10.1007/s00401-017-1803-x

Article  CAS 

Comments (0)

No login
gif