Nociceptor neurons affect cancer immunosurveillance.
Animals
Mice
Calcitonin Gene-Related Peptide
/ metabolism
CD8-Positive T-Lymphocytes
/ immunology
Melanoma
/ immunology
Nociceptors
/ physiology
Sensory Receptor Cells
/ metabolism
Neurites
/ metabolism
Lymphocytes, Tumor-Infiltrating
/ immunology
Survival Rate
Melanoma, Experimental
/ immunology
Genes, RAG-1
/ genetics
Humans
Biopsy
Prognosis
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
Nov 2022
Nov 2022
Historique:
received:
09
06
2021
accepted:
21
09
2022
pubmed:
4
11
2022
medline:
15
11
2022
entrez:
3
11
2022
Statut:
ppublish
Résumé
Solid tumours are innervated by nerve fibres that arise from the autonomic and sensory peripheral nervous systems
Identifiants
pubmed: 36323780
doi: 10.1038/s41586-022-05374-w
pii: 10.1038/s41586-022-05374-w
pmc: PMC9646485
doi:
Substances chimiques
Calcitonin Gene-Related Peptide
JHB2QIZ69Z
Ramp1 protein, mouse
0
TRPV1 protein, mouse
0
RAMP1 protein, human
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
405-412Subventions
Organisme : NICHD NIH HHS
ID : P50 HD105351
Pays : United States
Organisme : NINDS NIH HHS
ID : R35 NS105076
Pays : United States
Organisme : NIGMS NIH HHS
ID : P20 GM103620
Pays : United States
Organisme : NIGMS NIH HHS
ID : P20 GM103548
Pays : United States
Informations de copyright
© 2022. The Author(s).
Références
Amit, M. et al. Loss of p53 drives neuron reprogramming in head and neck cancer. Nature 578, 449–454 (2020).
pubmed: 32051587
doi: 10.1038/s41586-020-1996-3
Magnon, C. et al. Autonomic nerve development contributes to prostate cancer progression. Science 341, 1236361 (2013).
pubmed: 23846904
doi: 10.1126/science.1236361
Mauffrey, P. et al. Progenitors from the central nervous system drive neurogenesis in cancer. Nature 569, 672–678 (2019).
pubmed: 31092925
doi: 10.1038/s41586-019-1219-y
Zahalka, A. H. et al. Adrenergic nerves activate an angio-metabolic switch in prostate cancer. Science 358, 321–326 (2017).
pubmed: 29051371
pmcid: 5783182
doi: 10.1126/science.aah5072
Zahalka, A. H. & Frenette, P. S. Nerves in cancer. Nat. Rev. Cancer 20, 143–157 (2020).
pubmed: 31974491
pmcid: 7709871
doi: 10.1038/s41568-019-0237-2
Chambers, C. A., Kuhns, M. S., Egen, J. G. & Allison, J. P. CTLA-4-mediated inhibition in regulation of T cell responses: mechanisms and manipulation in tumor immunotherapy. Annu. Rev. Immunol. 19, 565–594 (2001).
pubmed: 11244047
doi: 10.1146/annurev.immunol.19.1.565
Das, M., Zhu, C. & Kuchroo, V. K. Tim-3 and its role in regulating anti-tumor immunity. Immunol. Rev. 276, 97–111 (2017).
pubmed: 28258697
pmcid: 5512889
doi: 10.1111/imr.12520
Topalian, S. L. et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366, 2443–2454 (2012).
pubmed: 22658127
pmcid: 3544539
doi: 10.1056/NEJMoa1200690
Baumeister, S. H., Freeman, G. J., Dranoff, G. & Sharpe, A. H. Coinhibitory pathways in immunotherapy for cancer. Annu. Rev. Immunol. 34, 539–573 (2016).
pubmed: 26927206
doi: 10.1146/annurev-immunol-032414-112049
Dougan, M. & Dranoff, G. Immune therapy for cancer. Annu. Rev. Immunol. 27, 83–117 (2009).
pubmed: 19007331
doi: 10.1146/annurev.immunol.021908.132544
Donnelly, C. R. et al. STING controls nociception via type I interferon signalling in sensory neurons. Nature 591, 275–280 (2021).
pubmed: 33442058
pmcid: 7977781
doi: 10.1038/s41586-020-03151-1
McIlvried, L. A., Atherton, M. A., Horan, N. L., Goch, T. N. & Scheff, N. N. Sensory neurotransmitter calcitonin gene-related peptide modulates tumor growth and lymphocyte infiltration in oral squamous cell carcinoma. Adv. Biol. 6, e2200019 (2022).
doi: 10.1002/adbi.202200019
Wang, K. et al. STING suppresses bone cancer pain via immune and neuronal modulation. Nat. Commun. 12, 4558 (2021).
pubmed: 34315904
pmcid: 8316360
doi: 10.1038/s41467-021-24867-2
Chen, G. et al. PD-L1 inhibits acute and chronic pain by suppressing nociceptive neuron activity via PD-1. Nat. Neurosci. 20, 917–926 (2017).
pubmed: 28530662
pmcid: 5831162
doi: 10.1038/nn.4571
Kamiya, A. et al. Genetic manipulation of autonomic nerve fiber innervation and activity and its effect on breast cancer progression. Nat. Neurosci. 22, 1289–1305 (2019).
pubmed: 31285612
doi: 10.1038/s41593-019-0430-3
Saloman, J. L. et al. Ablation of sensory neurons in a genetic model of pancreatic ductal adenocarcinoma slows initiation and progression of cancer. Proc. Natl Acad. Sci. USA 113, 3078–3083 (2016).
pubmed: 26929329
pmcid: 4801275
doi: 10.1073/pnas.1512603113
Talbot, S. et al. Silencing nociceptor neurons reduces allergic airway inflammation. Neuron 87, 341–354 (2015).
pubmed: 26119026
pmcid: 4506220
doi: 10.1016/j.neuron.2015.06.007
Anderson, P. & Gonzalez-Rey, E. Vasoactive intestinal peptide induces cell cycle arrest and regulatory functions in human T cells at multiple levels. Mol. Cell. Biol. 30, 2537–2551 (2010).
pubmed: 20231362
pmcid: 2863702
doi: 10.1128/MCB.01282-09
Haqq, C. et al. The gene expression signatures of melanoma progression. Proc. Natl Acad. Sci. USA 102, 6092–6097 (2005).
pubmed: 15833814
pmcid: 1087936
doi: 10.1073/pnas.0501564102
Harlin, H. et al. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res. 69, 3077–3085 (2009).
pubmed: 19293190
doi: 10.1158/0008-5472.CAN-08-2281
Riker, A. I. et al. The gene expression profiles of primary and metastatic melanoma yields a transition point of tumor progression and metastasis. BMC Med. Genom.1, 13 (2008).
doi: 10.1186/1755-8794-1-13
Talantov, D. et al. Novel genes associated with malignant melanoma but not benign melanocytic lesions. Clin. Cancer Res. 11, 7234–7242 (2005).
pubmed: 16243793
doi: 10.1158/1078-0432.CCR-05-0683
Hannila, S. S. et al. Secretory leukocyte protease inhibitor reverses inhibition by CNS myelin, promotes regeneration in the optic nerve, and suppresses expression of the transforming growth factor-β signaling protein Smad2. J. Neurosci. 33, 5138–5151 (2013).
pubmed: 23516280
pmcid: 3684282
doi: 10.1523/JNEUROSCI.5321-12.2013
Mueller, A. M. et al. Novel role for SLPI in MOG-induced EAE revealed by spinal cord expression analysis. J. Neuroinflammation 5, 20 (2008).
pubmed: 18501024
pmcid: 2438345
doi: 10.1186/1742-2094-5-20
Boilly, B., Faulkner, S., Jobling, P. & Hondermarck, H. Nerve dependence: from regeneration to cancer. Cancer Cell 31, 342–354 (2017).
pubmed: 28292437
doi: 10.1016/j.ccell.2017.02.005
Zhao, C. M. et al. Denervation suppresses gastric tumorigenesis. Sci. Transl. Med. 6, 250ra115 (2014).
pubmed: 25143365
pmcid: 4374618
doi: 10.1126/scitranslmed.3009569
Larkin, J. et al. Five-year survival with combined nivolumab and ipilimumab in advanced melanoma. N. Engl. J. Med. 381, 1535–1546 (2019).
pubmed: 31562797
doi: 10.1056/NEJMoa1910836
Wang, J. et al. UV-induced somatic mutations elicit a functional T cell response in the YUMMER1.7 mouse melanoma model. Pigment Cell Melanoma Res. 30, 428–435 (2017).
pubmed: 28379630
pmcid: 5820096
doi: 10.1111/pcmr.12591
Meeth, K., Wang, J. X., Micevic, G., Damsky, W. & Bosenberg, M. W. The YUMM lines: a series of congenic mouse melanoma cell lines with defined genetic alterations. Pigment Cell Melanoma Res. 29, 590–597 (2016).
pubmed: 27287723
pmcid: 5331933
doi: 10.1111/pcmr.12498
Cohen, J. A. et al. Cutaneous TRPV1
pubmed: 31353219
pmcid: 6788801
doi: 10.1016/j.cell.2019.06.022
Michoud, F. et al. Epineural optogenetic activation of nociceptors initiates and amplifies inflammation. Nat. Biotechnol. 39, 179–185 (2021).
pubmed: 32958958
doi: 10.1038/s41587-020-0673-2
Pellett, S., Tepp, W. H., Whitemarsh, R. C., Bradshaw, M. & Johnson, E. A. In vivo onset and duration of action varies for botulinum neurotoxin A subtypes 1–5. Toxicon 107, 37–42 (2015).
pubmed: 26130522
pmcid: 4658214
doi: 10.1016/j.toxicon.2015.06.021
Pinho-Ribeiro, F. A. et al. Blocking neuronal signaling to immune cells treats streptococcal invasive infection. Cell 173, 1083–1097 (2018).
pubmed: 29754819
pmcid: 5959783
doi: 10.1016/j.cell.2018.04.006
Binshtok, A. M., Bean, B. P. & Woolf, C. J. Inhibition of nociceptors by TRPV1-mediated entry of impermeant sodium channel blockers. Nature 449, 607–610 (2007).
pubmed: 17914397
doi: 10.1038/nature06191
Baral, P. et al. Nociceptor sensory neurons suppress neutrophil and γδ T cell responses in bacterial lung infections and lethal pneumonia. Nat. Med. 24, 417–426 (2018).
pubmed: 29505031
pmcid: 6263165
doi: 10.1038/nm.4501
Yissachar, N. et al. An intestinal organ culture system uncovers a role for the nervous system in microbe–immune crosstalk. Cell 168, 1135–1148 (2017).
pubmed: 28262351
pmcid: 5396461
doi: 10.1016/j.cell.2017.02.009
Chiu, I. M. et al. Bacteria activate sensory neurons that modulate pain and inflammation. Nature 501, 52–57 (2013).
pubmed: 23965627
pmcid: 3773968
doi: 10.1038/nature12479
Ding, W., Stohl, L. L., Wagner, J. A. & Granstein, R. D. Calcitonin gene-related peptide biases Langerhans cells toward Th2-type immunity. J. Immunol. 181, 6020–6026 (2008).
pubmed: 18941191
doi: 10.4049/jimmunol.181.9.6020
Kashem, S. W. et al. Nociceptive sensory fibers drive interleukin-23 production from CD301b+ Dermal dendritic cells and drive protective cutaneous immunity. Immunity 43, 515–526 (2015).
pubmed: 26377898
pmcid: 4607048
doi: 10.1016/j.immuni.2015.08.016
The Cancer Genome Atlas Research Network et al. The Cancer Genome Atlas Pan-Cancer analysis project. Nat. Genet. 45, 1113–1120 (2013).
doi: 10.1038/ng.2764
Jerby-Arnon, L. et al. A cancer cell program promotes T Cell exclusion and resistance to checkpoint blockade. Cell 175, 984–997 (2018).
pubmed: 30388455
pmcid: 6410377
doi: 10.1016/j.cell.2018.09.006
Tirosh, I. et al. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Science 352, 189–196 (2016).
pubmed: 27124452
pmcid: 4944528
doi: 10.1126/science.aad0501
Hogquist, K. A. et al. T cell receptor antagonist peptides induce positive selection. Cell 76, 17–27 (1994).
pubmed: 8287475
doi: 10.1016/0092-8674(94)90169-4
Crosson, T. et al. FcεR1-expressing nociceptors trigger allergic airway inflammation. J. Allergy Clin. Immunol. 147, 2330–2342 (2021).
pubmed: 33453289
pmcid: 9004488
doi: 10.1016/j.jaci.2020.12.644
Madisen, L. et al. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat. Neurosci. 15, 793–802 (2012).
pubmed: 22446880
pmcid: 3337962
doi: 10.1038/nn.3078
Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133–140 (2010).
pubmed: 20023653
doi: 10.1038/nn.2467
Voehringer, D., Liang, H. E. & Locksley, R. M. Homeostasis and effector function of lymphopenia-induced "memory-like" T cells in constitutively T cell-depleted mice. J. Immunol. 180, 4742–4753 (2008).
pubmed: 18354198
doi: 10.4049/jimmunol.180.7.4742
Lou, S. et al. Genetically targeted all-optical electrophysiology with a transgenic cre-dependent optopatch mouse. J. Neurosci. 36, 11059–11073 (2016).
pubmed: 27798186
pmcid: 5098841
doi: 10.1523/JNEUROSCI.1582-16.2016
Agarwal, N., Offermanns, S. & Kuner, R. Conditional gene deletion in primary nociceptive neurons of trigeminal ganglia and dorsal root ganglia. Genesis 38, 122–129 (2004).
pubmed: 15048809
doi: 10.1002/gene.20010
Fidler, I. J. Biological behavior of malignant melanoma cells correlated to their survival in vivo. Cancer Res. 35, 218–224 (1975).
pubmed: 1109790
Fidler, I. J. & Kripke, M. L. Metastasis results from preexisting variant cells within a malignant tumor. Science 197, 893–895 (1977).
pubmed: 887927
doi: 10.1126/science.887927
Headley, M. B. et al. Visualization of immediate immune responses to pioneer metastatic cells in the lung. Nature 531, 513–517 (2016).
pubmed: 26982733
pmcid: 4892380
doi: 10.1038/nature16985
Twyman-Saint Victor, C. et al. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 520, 373–377 (2015).
pubmed: 25754329
doi: 10.1038/nature14292
Huang, S. et al. Lymph nodes are innervated by a unique population of sensory neurons with immunomodulatory potential. Cell 184, 441–459 (2021).
pubmed: 33333021
doi: 10.1016/j.cell.2020.11.028
Renier, N. et al. iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159, 896–910 (2014).
pubmed: 25417164
doi: 10.1016/j.cell.2014.10.010
Broz, M. L. et al. Dissecting the tumor myeloid compartment reveals rare activating antigen-presenting cells critical for T cell immunity. Cancer Cell 26, 638–652 (2014).
pubmed: 25446897
pmcid: 4254577
doi: 10.1016/j.ccell.2014.09.007
Stathopoulou, C. et al. PD-1 inhibitory receptor downregulates asparaginyl endopeptidase and maintains Foxp3 transcription factor stability in induced regulatory T cells. Immunity 49, 247–263 (2018).
pubmed: 30054205
pmcid: 6105434
doi: 10.1016/j.immuni.2018.05.006
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Barrett, T. et al. NCBI GEO: archive for functional genomics data sets–update. Nucleic Acids Res. 41, D991–995 (2013).
pubmed: 23193258
doi: 10.1093/nar/gks1193
Chaplan, S. R., Bach, F. W., Pogrel, J. W., Chung, J. M. & Yaksh, T. L. Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods 53, 55–63 (1994).
pubmed: 7990513
doi: 10.1016/0165-0270(94)90144-9
Hargreaves, K., Dubner, R., Brown, F., Flores, C. & Joris, J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32, 77–88 (1988).
pubmed: 3340425
doi: 10.1016/0304-3959(88)90026-7
Pool, M., Thiemann, J., Bar-Or, A. & Fournier, A. E. NeuriteTracer: a novel ImageJ plugin for automated quantification of neurite outgrowth. J. Neurosci. Methods 168, 134–139 (2008).
pubmed: 17936365
doi: 10.1016/j.jneumeth.2007.08.029
Garcia-Segura, L. M. & Perez-Marquez, J. A new mathematical function to evaluate neuronal morphology using the Sholl analysis. J. Neurosci. Methods 226, 103–109 (2014).
pubmed: 24503022
doi: 10.1016/j.jneumeth.2014.01.016
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
pubmed: 24227677
doi: 10.1093/bioinformatics/btt656
Crosson, T. et al. Profiling of how nociceptor neurons detect danger—new and old foes. J. Intern. Med. 286, 268–289 (2019).
pubmed: 31282104
doi: 10.1111/joim.12957
Kupari, J., Haring, M., Agirre, E., Castelo-Branco, G. & Ernfors, P. An atlas of vagal sensory neurons and their molecular specialization. Cell Rep. 27, 2508–2523 (2019).
pubmed: 31116992
pmcid: 6533201
doi: 10.1016/j.celrep.2019.04.096
Usoskin, D. et al. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat. Neurosci. 18, 145–153 (2015).
pubmed: 25420068
doi: 10.1038/nn.3881
Li, C., Wang, S., Chen, Y. & Zhang, X. Somatosensory neuron typing with high-coverage single-cell RNA sequencing and functional analysis. Neurosci. Bull. 34, 200–207 (2018).
pubmed: 28612318
doi: 10.1007/s12264-017-0147-9
Chiu, I. M. et al. Transcriptional profiling at whole population and single cell levels reveals somatosensory neuron molecular diversity. eLife 3, e04660 (2014).
pmcid: 4383053
doi: 10.7554/eLife.04660
Goswami, S. C. et al. Molecular signatures of mouse TRPV1-lineage neurons revealed by RNA-seq transcriptome analysis. J. Pain 15, 1338–1359 (2014).
pubmed: 25281809
pmcid: 5469214
doi: 10.1016/j.jpain.2014.09.010
Ray, P. et al. Comparative transcriptome profiling of the human and mouse dorsal root ganglia: an RNA-seq-based resource for pain and sensory neuroscience research. Pain 159, 1325–1345 (2018).
pubmed: 29561359
pmcid: 6008200
doi: 10.1097/j.pain.0000000000001217
Monaco, G. et al. RNA-seq signatures normalized by mRNA abundance allow absolute deconvolution of human immune cell types. Cell Rep. 26, 1627–1640 (2019).
pubmed: 30726743
pmcid: 6367568
doi: 10.1016/j.celrep.2019.01.041
Castle, J. C. et al. Exploiting the mutanome for tumor vaccination. Cancer Res. 72, 1081–1091 (2012).
pubmed: 22237626
doi: 10.1158/0008-5472.CAN-11-3722
Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M. & Altman, D. G. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. J. Pharmacol. Pharmacother. 1, 94–99 (2010).
pubmed: 21350617
pmcid: 3043335
doi: 10.4103/0976-500X.72351
Heng, T. S. et al. The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol. 9, 1091–1094 (2008).
pubmed: 18800157
doi: 10.1038/ni1008-1091