Intracerebellar administration of the chemokine Cxcl3 reduces the volume of medulloblastoma lesions at an advanced stage by promoting the migration and differentiation of preneoplastic precursor cells.
Cxcl3 chemokine
Cxcr2 receptor
cell migration
human biopsies
medulloblastoma
mouse models
Journal
Brain pathology (Zurich, Switzerland)
ISSN: 1750-3639
Titre abrégé: Brain Pathol
Pays: Switzerland
ID NLM: 9216781
Informations de publication
Date de publication:
30 Jun 2024
30 Jun 2024
Historique:
received:
26
10
2023
accepted:
18
06
2024
medline:
1
7
2024
pubmed:
1
7
2024
entrez:
1
7
2024
Statut:
aheadofprint
Résumé
The prognosis for many pediatric brain tumors, including cerebellar medulloblastoma (MB), remains dismal but there is promise in new therapies. We have previously generated a mouse model developing spontaneous MB at high frequency, Ptch1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13283Subventions
Organisme : Fondazione Giovanni Celeghin
Organisme : Fondazione Adriano Buzzati-Traverso
Organisme : Ministero della Salute
Organisme : Italian Ministry of Universities and Research
Informations de copyright
© 2024 The Author(s). Brain Pathology published by John Wiley & Sons Ltd on behalf of International Society of Neuropathology.
Références
Zlotnik A, Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity. 2000;12:121–127. https://doi.org/10.1016/s1074-7613(00)80165-x
Hughes CE, Nibbs RJB. A guide to chemokines and their receptors. FEBS J. 2018;285:2944–2971. https://doi.org/10.1111/febs.14466
Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol. 2000;18:217–242. https://doi.org/10.1146/annurev.immunol.18.1.217
Adler MW, Rogers TJ. Are chemokines the third major system in the brain? J Leukoc Biol. 2005;78:1204–1209. https://doi.org/10.1189/jlb.0405222
Sowa JE, Tokarski K. Cellular, synaptic, and network effects of chemokines in the central nervous system and their implications to behavior. Pharmacol Rep. 2021;73:1595–1625. https://doi.org/10.1007/s43440-021-00323-2
de Haas AH, van Weering HR, de Jong EK, Boddeke HW, Biber KP. Neuronal chemokines: versatile messengers in central nervous system cell interaction. Mol Neurobiol. 2007;36:137–151. https://doi.org/10.1007/s12035-007-0036-8
i Altaba AR, Palma V, Dahmane N. Hedgehog‐Gli signalling and the growth of the brain. Nat Rev Neurosci. 2002;3:24–33. https://doi.org/10.1038/nrn704
Gillard SE, Lu M, Mastracci RM, Miller RJ. Expression of functional chemokine receptors by rat cerebellar neurons. J Neuroimmunol. 2002;124:16–28. https://doi.org/10.1016/s0165-5728(02)00005-x
Meng SZ, Oka A, Takashima S. Developmental expression of monocyte chemoattractant protein‐1 in the human cerebellum and brainstem. Brain Dev. 1999;21:30–35. https://doi.org/10.1016/s0387-7604(98)00065-5
van Gassen KL, Netzeband JG, de Graan PN, Gruol DL. The chemokine CCL2 modulates Ca2+ dynamics and electrophysiological properties of cultured cerebellar Purkinje neurons. Eur J Neurosci. 2005;21:2949–2957. https://doi.org/10.1111/j.1460-9568.2005.04113.x
Giovannelli A, Limatola C, Ragozzino D, Mileo AM, Ruggieri A, Ciotti MT, et al. CXC chemokines interleukin‐8 (IL‐8) and growth‐related gene product alpha (GROalpha) modulate Purkinje neuron activity in mouse cerebellum. J Neuroimmunol. 1998;92:122–132. https://doi.org/10.1016/s0165-5728(98)00192-1
Limatola C, Giovannelli A, Maggi L, Ragozzino D, Castellani L, Ciotti MT, et al. SDF‐1alpha‐mediated modulation of synaptic transmission in rat cerebellum. Eur J Neurosci. 2000;12:2497–2504. https://doi.org/10.1046/j.1460-9568.2000.00139.x
Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, et al. Impaired B‐lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4‐ and SDF‐1‐deficient mice. Proc Natl Acad Sci U S A. 1998;95:9448–9453. https://doi.org/10.1073/pnas.95.16.9448
Zhu Y, Yu T, Zhang XC, Nagasawa T, Wu JY, Rao Y. Role of the chemokine SDF‐1 as the meningeal attractant for embryonic cerebellar neurons. Nat Neurosci. 2002;5:719–720. https://doi.org/10.1038/nn881
Farioli‐Vecchioli S, Cinà I, Ceccarelli M, Micheli L, Leonardi L, Ciotti MT, et al. Tis21 knock‐out enhances the frequency of medulloblastoma in Patched1 heterozygous mice by inhibiting the Cxcl3‐dependent migration of cerebellar neurons. J Neurosci. 2012;32:15547–15564. https://doi.org/10.1523/JNEUROSCI.0412-12.2012
Kumar V, Kumar V, McGuire T, Coulter DW, Sharp JG, Mahato RI. Challenges and recent advances in medulloblastoma therapy. Trends Pharmacol Sci. 2017;38:1061–1084. https://doi.org/10.1016/j.tips.2017.09.002
Northcott PA, Robinson GW, Kratz CP, Mabbott DJ, Pomeroy SL, Clifford SC, et al. Medulloblastoma. Nat Rev Dis Primers. 2019;5:11. https://doi.org/10.1038/s41572-019-0063-6
Juraschka K, Taylor MD. Medulloblastoma in the age of molecular subgroups: a review. J Neurosurg Pediatr. 2019;24:353–363. https://doi.org/10.3171/2019.5.PEDS18381
Kieffer V, Chevignard MP, Dellatolas G, Puget S, Dhermain F, Grill J, et al. Intellectual, educational, and situation‐based social outcome in adult survivors of childhood medulloblastoma. Dev Neurorehabil. 2019;22:19–26. https://doi.org/10.1080/17518423.2018.1424262
King AA, Seidel K, Di C, Leisenring WM, Perkins SM, Krull KR, et al. Long‐term neurologic health and psychosocial function of adult survivors of childhood medulloblastoma/PNET: a report from the childhood cancer survivor study. Neuro Oncol. 2017;19:689–698. https://doi.org/10.1093/neuonc/now242
Moxon‐Emre I, Bouffet E, Taylor MD, Laperriere N, Scantlebury N, Law N, et al. Impact of craniospinal dose, boost volume, and neurologic complications on intellectual outcome in patients with medulloblastoma. J Clin Oncol. 2014;32:1760–1768. https://doi.org/10.1200/JCO.2013.52.3290
Ceccarelli M, Micheli L, Tirone F. Suppression of medulloblastoma lesions by forced migration of preneoplastic precursor cells with intracerebellar administration of the chemokine Cxcl3. Front Pharmacol. 2016;7:484. https://doi.org/10.3389/fphar.2016.00484
Kessler JD, Hasegawa H, Brun SN, Emmenegger BA, Yang ZJ, Dutton JW, et al. N‐myc alters the fate of preneoplastic cells in a mouse model of medulloblastoma. Genes Dev. 2009;23:157–170. https://doi.org/10.1101/gad.1759909
Hahn H, Wojnowski L, Zimmer AM, Hall J, Miller G, Zimmer A. Rhabdomyosarcomas and radiation hypersensitivity in a mouse model of Gorlin syndrome. Nat Med. 1998;4:619–622. https://doi.org/10.1038/nm0598-619
Park S, Lee YJ, Lee HJ, Seki T, Hong KH, Park J, et al. B‐cell translocation gene 2 (Btg2) regulates vertebral patterning by modulating bone morphogenetic protein/smad signaling. Mol Cell Biol. 2004;24:10256–10262. https://doi.org/10.1128/MCB.24.23.10256-10262.2004
Ceccarelli M, D'Andrea G, Micheli L, Gentile G, Cavallaro S, Merlino G, et al. Tumor growth in the high frequency medulloblastoma mouse model Ptch1+/‐/Tis21KO has a specific activation signature of the PI3K/AKT/mTOR pathway and is counteracted by the PI3K inhibitor MEN1611. Front Oncol. 2021;11:692053. https://doi.org/10.3389/fonc.2021.692053
Ceccarelli M, D'Andrea G, Micheli L, Tirone F. Deletion of Btg1 induces Prmt1‐dependent apoptosis and increased stemness in Shh‐type medulloblastoma cells without affecting tumor frequency. Front Oncol. 2020;10:226. https://doi.org/10.3389/fonc.2020.00226
Ceccarelli M, Micheli L, D'Andrea G, De Bardi M, Scheijen B, Ciotti M, et al. Altered cerebellum development and impaired motor coordination in mice lacking the Btg1 gene: involvement of cyclin D1. Dev Biol. 2015;408:109–125. https://doi.org/10.1016/j.ydbio.2015.10.007
Onvani S, Terakawa Y, Smith C, Northcott P, Taylor M, Rutka J. Molecular genetic analysis of the hepatocyte growth factor/MET signaling pathway in pediatric medulloblastoma. Genes Chromosomes Cancer. 2012;51:675–688. https://doi.org/10.1002/gcc.21954
Abouantoun TJ, MacDonald TJ. Imatinib blocks migration and invasion of medulloblastoma cells by concurrently inhibiting activation of platelet‐derived growth factor receptor and transactivation of epidermal growth factor receptor. Mol Cancer Ther. 2009;8:1137–1147. https://doi.org/10.1158/1535-7163.MCT-08-0889
Pan W, Song XY, Hu QB, Zhang M, Xu XH. TSP2 acts as a suppresser of cell invasion, migration and angiogenesis in medulloblastoma by inhibiting the notch signaling pathway. Brain Res. 2019;1718:223–230. https://doi.org/10.1016/j.brainres.2019.05.004
Wen J, Zhao Z, Huang L, Wang L, Miao Y, Wu J. IL‐8 promotes cell migration through regulating EMT by activating the Wnt/β‐catenin pathway in ovarian cancer. J Cell Mol Med. 2020;24:1588–1598. https://doi.org/10.1111/jcmm.14848
Asadzadeh F, Ferrucci V, Antonellis PDE, Zollo M. In vivo bioluminescence imaging using orthotopic xenografts towards patient's derived‐xenograft medulloblastoma models. Q J Nucl Med Mol Imaging. 2017;61:95–101. https://doi.org/10.23736/S1824-4785.16.02959-9
Ferrucci V, de Antonellis P, Pennino FP, Asadzadeh F, Virgilio A, Montanaro D, et al. Metastatic group 3 medulloblastoma is driven by PRUNE1 targeting NME1‐TGF‐β‐OTX2‐SNAIL via PTEN inhibition. Brain. 2018;141:1300–1319. https://doi.org/10.1093/brain/awy039
Catanzaro G, Sabato C, Russo M, Rosa A, Abballe L, Besharat ZM, et al. Loss of miR‐107, miR‐181c and miR‐29a‐3p promote activation of Notch2 signaling in pediatric high‐grade gliomas (pHGGs). Int J Mol Sci. 2017;18:2742. https://doi.org/10.3390/ijms18122742
de Paula Alves Coelho KM, Stall J, Fronza Júnior H, Blasius R, de França PHC. Evaluation of expression of genes CADM1, TWIST1 and CDH1 by immunohistochemistry in melanocytic lesions. Pathol Res Pract. 2017;213:1067–1071. https://doi.org/10.1016/j.prp.2017.07.028
Weyer A, Schilling K. Developmental and cell type‐specific expression of the neuronal marker NeuN in the murine cerebellum. J Neurosci Res. 2003;73:400–409. https://doi.org/10.1002/jnr.10655
Porter AG, Jänicke RU. Emerging roles of caspase‐3 in apoptosis. Cell Death Differ. 1999;6:99–104. https://doi.org/10.1038/sj.cdd.4400476
Scholzen T, Gerdes J. The Ki‐67 protein: from the known and the unknown. J Cell Physiol. 2000;182:311–322. https://doi.org/10.1002/(SICI)1097-4652(200003)182:3<311::AID-JCP1>3.0.CO;2-9
Ivanov DP, Coyle B, Walker DA, Grabowska AM. In vitro models of medulloblastoma: choosing the right tool for the job. J Biotechnol. 2016;236:10–25. https://doi.org/10.1016/j.jbiotec.2016.07.028
Jacobsen PF, Jenkyn DJ, Papadimitriou JM. Establishment of a human medulloblastoma cell line and its heterotransplantation into nude mice. J Neuropathol Exp Neurol. 1985;44:472–485. https://doi.org/10.1097/00005072-198509000-00003
MacDonald TJ, Brown KM, LaFleur B, Peterson K, Lawlor C, Chen Y, et al. Expression profiling of medulloblastoma: PDGFRA and the RAS/MAPK pathway as therapeutic targets for metastatic disease. Nat Genet. 2001;29:143–152. https://doi.org/10.1038/ng731
Friedman HS, Burger PC, Bigner SH, Trojanowski JQ, Wikstrand CJ, Halperin EC, et al. Establishment and characterization of the human medulloblastoma cell line and transplantable xenograft D283 Med. J Neuropathol Exp Neurol. 1985;44:592–605. https://doi.org/10.1097/00005072-198511000-00005
Phoenix TN, Patmore DM, Boop S, Boulos N, Jacus MO, Patel YT, et al. Medulloblastoma genotype dictates blood brain barrier phenotype. Cancer Cell. 2016;29:508–522. https://doi.org/10.1016/j.ccell.2016.03.002
Yoneyama M, Shiba T, Hasebe S, Ogita K. Adult neurogenesis is regulated by endogenous factors produced during neurodegeneration. J Pharmacol Sci. 2011;115:425–432. https://doi.org/10.1254/jphs.11r02cp
Yang ZJ, Ellis T, Markant SL, Read TA, Kessler JD, Bourboulas M, et al. Medulloblastoma can be initiated by deletion of patched in lineage‐restricted progenitors or stem cells. Cancer Cell. 2008;14:135–145. https://doi.org/10.1016/j.ccr.2008.07.003
Wu D, LaRosa GJ, Simon MI. G protein‐coupled signal transduction pathways for interleukin‐8. Science. 1993;261:101–103. https://doi.org/10.1126/science.8316840
Rose JJ, Foley JF, Murphy PM, Venkatesan S. On the mechanism and significance of ligand‐induced internalization of human neutrophil chemokine receptors CXCR1 and CXCR2. J Biol Chem. 2004;279:24372–24386. https://doi.org/10.1074/jbc.M401364200
Luan J, Furuta Y, Du J, Richmond A. Developmental expression of two CXC chemokines, MIP‐2 and KC, and their receptors. Cytokine. 2001;14:253–263. https://doi.org/10.1006/cyto.2001.0882
Semple BD, Kossmann T, Morganti‐Kossmann MC. Role of chemokines in CNS health and pathology: a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. J Cereb Blood Flow Metab. 2010;30:459–473. https://doi.org/10.1038/jcbfm.2009.240
Vallès A, Grijpink‐Ongering L, de Bree FM, Tuinstra T, Ronken E. Differential regulation of the CXCR2 chemokine network in rat brain trauma: implications for neuroimmune interactions and neuronal survival. Neurobiol Dis. 2006;22:312–322. https://doi.org/10.1016/j.nbd.2005.11.015
Lax P, Limatola C, Fucile S, Trettel F, Di Bartolomeo S, Renzi M, et al. Chemokine receptor CXCR2 regulates the functional properties of AMPA‐type glutamate receptor GluR1 in HEK cells. J Neuroimmunol. 2002;129:66–73. https://doi.org/10.1016/s0165-5728(02)00178-9
Ha H, Debnath B, Neamati N. Role of the CXCL8‐CXCR1/2 axis in cancer and inflammatory diseases. Theranostics. 2017;7:1543–1588. https://doi.org/10.7150/thno.15625
Penco‐Campillo M, Molina C, Piris P, Soufi N, Carré M, Pagnuzzi‐Boncompagni M, et al. Targeting of the ELR+CXCL/CXCR1/2 pathway is a relevant strategy for the treatment of paediatric medulloblastomas. Cells. 2022;11:3933. https://doi.org/10.3390/cells11233933
Azzarelli R, Simons BD, Philpott A. The developmental origin of brain tumours: a cellular and molecular framework. Development. 2018;145:dev162693. https://doi.org/10.1242/dev.162693
Wu X, Northcott PA, Dubuc A, Dupuy AJ, Shih DJ, Witt H, et al. Clonal selection drives genetic divergence of metastatic medulloblastoma. Nature. 2012;482:529–533. https://doi.org/10.1038/nature10825
Yang WQ, Senger D, Muzik H, Shi ZQ, Johnson D, Brasher PM, et al. Reovirus prolongs survival and reduces the frequency of spinal and leptomeningeal metastases from medulloblastoma. Cancer Res. 2003;63:3162–3172.
Casciati A, Tanori M, Manczak R, Saada S, Tanno B, Giardullo P, et al. Human medulloblastoma cell lines: investigating on cancer stem cell‐like phenotype. Cancers (Basel). 2020;12:226. https://doi.org/10.3390/cancers12010226
Van Ommeren R, Garzia L, Holgado BL, Ramaswamy V, Taylor MD. The molecular biology of medulloblastoma metastasis. Brain Pathol. 2020;30:691–702. https://doi.org/10.1111/bpa.12811
Ramaswamy V, Remke M, Bouffet E, Faria CC, Perreault S, Cho YJ, et al. Recurrence patterns across medulloblastoma subgroups: an integrated clinical and molecular analysis. Lancet Oncol. 2013;14:1200–1207. https://doi.org/10.1016/S1470-2045(13)70449-2
Ellison DW, Onilude OE, Lindsey JC, Lusher ME, Weston CL, Taylor RE, et al. Beta‐catenin status predicts a favorable outcome in childhood medulloblastoma: the United Kingdom children's cancer study group brain tumour committee. J Clin Oncol. 2005;23:7951–7957. https://doi.org/10.1200/JCO.2005.01.5479
Nellan A, Rota C, Majzner R, Lester‐McCully CM, Griesinger AM, Mulcahy Levy JM, et al. Durable regression of medulloblastoma after regional and intravenous delivery of anti‐HER2 chimeric antigen receptor T cells. J Immunother Cancer. 2018;6:30. https://doi.org/10.1186/s40425-018-0340-z