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Citations to this article

Schwann cells induce cancer cell dispersion and invasion
Sylvie Deborde, … , Alan Hall, Richard J. Wong
Sylvie Deborde, … , Alan Hall, Richard J. Wong
Published March 21, 2016
Citation Information: J Clin Invest. 2016;126(4):1538-1554. https://doi.org/10.1172/JCI82658.
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Research Article Cell biology Oncology Article has an altmetric score of 3

Schwann cells induce cancer cell dispersion and invasion

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Abstract

Nerves enable cancer progression, as cancers have been shown to extend along nerves through the process of perineural invasion, which carries a poor prognosis. Furthermore, the innervation of some cancers promotes growth and metastases. It remains unclear, however, how nerves mechanistically contribute to cancer progression. Here, we demonstrated that Schwann cells promote cancer invasion through direct cancer cell contact. Histological evaluation of murine and human cancer specimens with perineural invasion uncovered a subpopulation of Schwann cells that associates with cancer cells. Coculture of cancer cells with dorsal root ganglion extracts revealed that Schwann cells direct cancer cells to migrate toward nerves and promote invasion in a contact-dependent manner. Upon contact, Schwann cells induced the formation of cancer cell protrusions in their direction and intercalated between the cancer cells, leading to cancer cell dispersion. The formation of these processes was dependent on Schwann cell expression of neural cell adhesion molecule 1 (NCAM1) and ultimately promoted perineural invasion. Moreover, NCAM1-deficient mice showed decreased neural invasion and less paralysis. Such Schwann cell behavior reflects normal Schwann cell programs that are typically activated in nerve repair but are instead exploited by cancer cells to promote perineural invasion and cancer progression.

Authors

Sylvie Deborde, Tatiana Omelchenko, Anna Lyubchik, Yi Zhou, Shizhi He, William F. McNamara, Natalya Chernichenko, Sei-Young Lee, Fernando Barajas, Chun-Hao Chen, Richard L. Bakst, Efsevia Vakiani, Shuangba He, Alan Hall, Richard J. Wong

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Year: 2025 2024 2023 2022 2021 2020 2019 2018 2017 2016 2009 Total
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A Ferdoushi, X Li, N Griffin, S Faulkner, MF Jamaluddin, F Gao, CC Jiang, DF van Helden, PS Tanwar, P Jobling, H Hondermarck
Frontiers in Oncology 2020
Schwann Cell-Derived CCL2 Promotes the Perineural Invasion of Cervical Cancer
T Huang, Q Fan, Y Wang, Y Cui, Z Wang, L Yang, X Sun, Y Wang
Frontiers in Oncology 2020
Future directions in preclinical and translational cancer neuroscience research
IE Demir, CM Reyes, W Alrawashdeh, GO Ceyhan, S Deborde, H Friess, K Görgülü, R Istvanffy, D Jungwirth, R Kuner, M Maryanovich, S Naara, S Renders, JL Saloman, NN Scheff, H Steenfadt, P Stupakov, V Thiel, D Verma, BS Yilmaz, RA White, TC Wang, RJ Wong, PS Frenette, Z Gil, BM Davis
2020
Cdc42 Mediates Cancer Cell Chemotaxis in Perineural Invasion
N Chernichenko, T Omelchenko, S Deborde, RL Bakst, S He, CH Chen, L Gusain, E Vakiani, N Katabi, A Hall, RJ Wong
Molecular cancer research : MCR 2020
Integrating the Tumor Microenvironment into Cancer Therapy
S Sanegre, F Lucantoni, R Burgos-Panadero, L de La Cruz-Merino, R Noguera, TÁ Naranjo
Cancers 2020
Establishment of a Convenient System for the Culture and Study of Perineurium Barrier In Vitro
X Yin, X Liu, Y Zhang, J Zeng, X Liang, X Yang, J Hou
Cellular and Molecular Neurobiology 2020
Perineural Invasion in Adenoid Cystic Carcinoma of the Salivary Glands: Where We Are and Where We Need to Go
X Liu, X Yang, C Zhan, Y Zhang, J Hou, X Yin
Frontiers in Oncology 2020
Tumor-neuroglia interaction promotes pancreatic cancer metastasis
D Su, X Guo, L Huang, H Ye, Z Li, L Lin, R Chen, Q Zhou
Theranostics 2020
Identification of three subtypes of triple-negative breast cancer with potential therapeutic implications
P Jézéquel, O Kerdraon, H Hondermarck, C Guérin-Charbonnel, H Lasla, W Gouraud, JL Canon, A Gombos, F Dalenc, S Delaloge, J Lemonnier, D Loussouarn, V Verrièle, M Campone
Breast Cancer Research 2019
Differentiation and maturation of oligodendrocytes in human three-dimensional neural cultures
RM Marton, Y Miura, SA Sloan, Q Li, O Revah, RJ Levy, JR Huguenard, SP Pașca
Nature Neuroscience 2019
Reciprocal interactions between cancer and Schwann cells contribute to oral cancer progression and pain
E Salvo, P Saraithong, JG Curtin, MN Janal, Y Ye
Heliyon 2019
Melanoma-induced reprogramming of Schwann cell signaling aids tumor growth
GV Shurin, O Kruglov, F Ding, Y Lin, X Hao, AA Keskinov, Z You, AE Lokshin, WA LaFramboise, LD Falo, MR Shurin, YL Bunimovich
Cancer research 2019
Perineural invasion in cervical cancer: pay attention to the indications of nerve-sparing radical hysterectomy
Y Zhu, GN Zhang, Y Shi, L Cui, XF Leng, JM Huang
Annals of translational medicine 2019
Nerves and Pancreatic Cancer: New Insights into a Dangerous Relationship
Gasparini, Pellegatta, Crippa, Lena, Belfiori, Doglioni, Taveggia, Falconi
Cancers 2019
Immunomodulation by Schwann cells in disease
SH Zhang, GV Shurin, H Khosravi, R Kazi, O Kruglov, MR Shurin, YL Bunimovich
Cancer Immunology, Immunotherapy 2019
Schwann cell reprogramming and lung cancer progression: a meta-analysis of transcriptome data
VM Silva, JA Gomes, LP Tenório, GC de Omena Neta, K da Costa Paixão, AK Duarte, GC da Silva, RJ Ferreira, BD Koike, C de Sales Marques, RD da Silva Miguel, AC de Queiroz, LX Pereira, CA de Carvalho Fraga
Oncotarget 2019
Schwann cells support oncogenic potential of pancreatic cancer cells through TGFβ signaling
E Roger, S Martel, A Bertrand-Chapel, A Depollier, N Chuvin, RM Pommier, K Yacoub, C Caligaris, V Cardot-Ruffino, V Chauvet, S Aires, K Mohkam, JY Mabrut, M Adham, T Fenouil, V Hervieu, L Broutier, M Castets, C Neuzillet, PA Cassier, R Tomasini, S Sentis, L Bartholin
Cell Death and Disease 2019
Schwann cells shape the neuro-immune environs and control cancer progression
GV Martyn, GV Shurin, AA Keskinov, YL Bunimovich, MR Shurin
Cancer Immunology, Immunotherapy 2019
Antibodies against cell adhesion molecules and neural structures in paraneoplastic neuropathies
AM Siles, E Martínez-Hernández, J Araque, J Diaz-Manera, R Rojas-Garcia, E Gallardo, I Illa, F Graus, L Querol
Annals of Clinical and Translational Neurology 2018
Perineural Invasion in Head and Neck Cancer
LB Schmitd, CS Scanlon, NJ DSilva
Journal of dental research 2018
Redefining Perineural Invasion: Integration of Biology With Clinical Outcome
LB Schmitd, LJ Beesley, N Russo, EL Bellile, RC Inglehart, M Liu, G Romanowicz, GT Wolf, JM Taylor, NJ D'Silva
Neoplasia (New York, N.Y.) 2018
L1CAM induces perineural invasion of pancreas cancer cells by upregulation of metalloproteinase expression
S Naara, M Amit, Z Gil
Oncogene 2018
An In Vivo Murine Sciatic Nerve Model of Perineural Invasion
S Deborde, Y Yu, A Marcadis, CH Chen, N Fan, RL Bakst, RJ Wong
Journal of visualized experiments : JoVE 2018
Inflammatory Monocytes Promote Perineural Invasion via CCL2-Mediated Recruitment and Cathepsin B Expression
RL Bakst, H Xiong, CH Chen, S Deborde, A Lyubchik, Y Zhou, S He, W McNamara, SY Lee, OC Olson, IM Leiner, AR Marcadis, JW Keith, HA Al-Ahmadie, N Katabi, Z Gil, E Vakiani, JA Joyce, E Pamer, RJ Wong
Cancer research 2017
How Schwann cells facilitate cancer progression in nerves
S Deborde, RJ Wong
Cellular and Molecular Life Sciences 2017
Colorectal Cancer Cells Adhere to and Migrate Along the Neurons of the Enteric Nervous System
E Duchalais, C Guilluy, S Nedellec, M Touvron, A Bessard, Y Touchefeu, C Bossard, H Boudin, G Louarn, M Neunlist, LV Landeghem
Cellular and Molecular Gastroenterology and Hepatology 2017
Cancer’s got nerve: Schwann cells drive perineural invasion
Chad Pecot, Salma Azam
Journal of Clinical Investigation 2016
The Cohesive Metastasis Phenotype in Human Prostate Cancer
WL Harryman, JP Hinton, CP Rubenstein, P Singh, RB Nagle, SJ Parker, BS Knudsen, AE Cress
Biochimica et Biophysica Acta (BBA) - Reviews on Cancer 2016
Can Stopping Nerves, Stop Cancer?
JL Saloman, KM Albers, AD Rhim, BM Davis
Trends in Neurosciences 2016
Schwann cells: a new player in the tumor microenvironment
YL Bunimovich, AA Keskinov, GV Shurin, MR Shurin
Cancer Immunology, Immunotherapy 2016
Mechanisms of Perineural Invasion
Bakst RL, Wong RJ
Journal of Neurological Surgery Part B Skull Base 2016
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 2009

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