Neural control of tumor immunity.
cancer
cancer neuroimmunology
immune system
nervous system
neuroimmunology
tumor immunology
Journal
The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646
Informations de publication
Date de publication:
20 Sep 2024
20 Sep 2024
Historique:
revised:
02
06
2024
received:
23
02
2024
accepted:
09
09
2024
medline:
21
9
2024
pubmed:
21
9
2024
entrez:
21
9
2024
Statut:
aheadofprint
Résumé
Communication between the nervous system and the immune system has evolved to optimally respond to potentially dangerous stimuli both from within and outside the body. Tumors pose a severe threat to an organism and current therapies are insufficient for tumor regression in the majority of cases. Studies show that tumors are innervated by peripheral nerves from the sensory, parasympathetic and sympathetic nervous systems. Interactions between cancer cells, nerves and immune cells regulate overall tumor progression. Clinical studies have indicated the potential of targeting the peripheral nervous system for promoting anti-tumor immune responses. This view point provides an opinion on the current evidence and therapeutic potential of manipulating neuro-immune communications in cancer.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : ERC Consolidator
ID : 101001233
Organisme : Swiss National Science Foundation
ID : 310030_182417/1
Pays : Switzerland
Organisme : Swiss Cancer League
ID : KLS-4836-08-2019
Organisme : Swiss Cancer League
ID : KLS-5898-08-2023
Organisme : Geneva Cancer League
ID : 2106
Organisme : German Research Foundation
ID : TRR359
Organisme : EU ITN
ID : 813284
Organisme : Human Frontier Science Program
ID : LT0051/2022-L
Informations de copyright
© 2024 The Author(s). The FEBS Journal published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
Références
Chu C, Artis D & Chiu IM (2020) Neuro‐immune interactions in the tissues. Immunity 52, 464–474.
De Virgiliis F, Oliva VM, Kizil B & Scheiermann C (2022) Control of lymph node activity by direct local innervation. Trends Neurosci 45, 704–712.
Klein Wolterink RGJ, Wu GS, Chiu IM & Veiga‐Fernandes H (2022) Neuroimmune interactions in peripheral organs. Annu Rev Neurosci 45, 339–360.
Baraldi JH, Martyn GV, Shurin GV & Shurin MR (2022) Tumor innervation: history, methodologies, and significance. Cancers 14, 1979.
Magnon C, Hall SJ, Lin J, Xue X, Gerber L, Freedland SJ & Frenette PS (2013) Autonomic nerve development contributes to prostate cancer progression. Science 341, 1236361.
Zahalka AH & Frenette PS (2020) Nerves in cancer. Nat Rev Cancer 20, 143–157.
Wang W, Li L, Chen N, Niu C, Li Z, Hu J & Cui J (2020) Nerves in the tumor microenvironment: origin and effects. Front Cell Dev Biol 8, 601738.
Le TT & Oudin MJ (2023) Understanding and modeling nerve‐cancer interactions. Dis Model Mech 16, dmm049729.
Uesaka T, Young HM, Pachnis V & Enomoto H (2016) Development of the intrinsic and extrinsic innervation of the gut. Dev Biol 417, 158–167.
Robinson DR, McNaughton PA, Evans ML & Hicks GA (2004) Characterization of the primary spinal afferent innervation of the mouse colon using retrograde labelling. Neurogastroenterol Motil 16, 113–124.
Spencer NJ & Hu H (2020) Enteric nervous system: sensory transduction, neural circuits and gastrointestinal motility. Nat Rev Gastroenterol Hepatol 17, 338–351.
Tan LL, Bornstein JC & Anderson CR (2008) Distinct chemical classes of medium‐sized transient receptor potential channel vanilloid 1‐immunoreactive dorsal root ganglion neurons innervate the adult mouse jejunum and colon. Neuroscience 156, 334–343.
Magnon C & Hondermarck H (2023) The neural addiction of cancer. Nat Rev Cancer 23, 317–334.
Bosch‐Queralt M, Fledrich R & Stassart RM (2023) Schwann cell functions in peripheral nerve development and repair. Neurobiol Dis 176, 105952.
Huang S, Ziegler CGK, Austin J, Mannoun N, Vukovic M, Ordovas‐Montanes J, Shalek AK & von Andrian UH (2021) Lymph nodes are innervated by a unique population of sensory neurons with immunomodulatory potential. Cell 184, 441–459.e25.
Faulkner S, Jobling P, March B, Jiang CC & Hondermarck H (2019) Tumor neurobiology and the war of nerves in cancer. Cancer Discov 9, 702–710.
Kamiya A, Hiyama T, Fujimura A & Yoshikawa S (2021) Sympathetic and parasympathetic innervation in cancer: therapeutic implications. Clin Auton Res 31, 165–178.
Yin L, Li J, Wang J, Pu T, Wei J, Li Q & Wu BJ (2021) MAOA promotes prostate cancer cell perineural invasion through SEMA3C/PlexinA2/NRP1‐cMET signaling. Oncogene 40, 1362–1374.
Espana‐Ferrufino A, Lino‐Silva LS & Salcedo‐Hernandez RA (2018) Extramural Perineural invasion in pT3 and pT4 gastric carcinomas. J Pathol Transl Med 52, 79–84.
Oven Ustaalioglu BB, Bilici A, Seker M, Kefeli U, Aydin D, Celik S, Demir T & Erkol B (2019) Prognostic factors for operated gallbladder cancer. J Gastrointest Cancer 50, 451–457.
Geng Q, Li L, Shen Z, Zheng Y, Wang L, Xue R, Xue W, Peng M & Zhao J (2023) Norepinephrine inhibits CD8(+) T‐cell infiltration and function, inducing anti‐PD‐1 mAb resistance in lung adenocarcinoma. Br J Cancer 128, 1223–1235.
Schmitd LB, Scanlon CS & D'Silva NJ (2018) Perineural invasion in head and neck cancer. J Dent Res 97, 742–750.
Zhu Y, Zhang G, Yang Y, Cui L, Jia S, Shi Y, Song S & Xu S (2018) Perineural invasion in early‐stage cervical cancer and its relevance following surgery. Oncol Lett 15, 6555–6561.
Li X, Peng X, Yang S, Wei S, Fan Q, Liu J, Yang L & Li H (2022) Targeting tumor innervation: premises, promises, and challenges. Cell Death Dis 8, 131.
Bapat AA, Hostetter G, Von Hoff DD & Han H (2011) Perineural invasion and associated pain in pancreatic cancer. Nat Rev Cancer 11, 695–707.
Demir IE, Friess H & Ceyhan GO (2012) Nerve‐cancer interactions in the stromal biology of pancreatic cancer. Front Physiol 3, 97.
Huang Y, He L, Dong D, Yang C, Liang C, Chen X, Ma Z, Huang X, Yao S, Liang C et al. (2018) Individualized prediction of perineural invasion in colorectal cancer: development and validation of a radiomics prediction model. Chin J Cancer Res 30, 40–50.
Mancusi R & Monje M (2023) The neuroscience of cancer. Nature 618, 467–479.
Monje M, Borniger JC, D'Silva NJ, Deneen B, Dirks PB, Fattahi F, Frenette PS, Garzia L, Gutmann DH, Hanahan D et al. (2020) Roadmap for the emerging field of cancer neuroscience. Cell 181, 219–222.
Balood M, Ahmadi M, Eichwald T, Ahmadi A, Majdoubi A, Roversi K, Roversi K, Lucido CT, Restaino AC, Huang S et al. (2022) Nociceptor neurons affect cancer immunosurveillance. Nature 611, 405–412.
Saloman JL, Albers KM, Li D, Hartman DJ, Crawford HC, Muha EA, Rhim AD & Davis BM (2016) 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.
Vats K, Kruglov O, Sahoo B, Soman V, Zhang J, Shurin GV, Chandran UR, Skums P, Shurin MR, Zelikovsky A et al. (2022) Sensory nerves impede the formation of tertiary lymphoid structures and development of protective Antimelanoma immune responses. Cancer Immunol Res 10, 1141–1154.
Peterson SC, Eberl M, Vagnozzi AN, Belkadi A, Veniaminova NA, Verhaegen ME, Bichakjian CK, Ward NL, Dlugosz AA & Wong SY (2015) Basal cell carcinoma preferentially arises from stem cells within hair follicle and mechanosensory niches. Cell Stem Cell 16, 400–412.
Douglas SD & Leeman SE (2011) Neurokinin‐1 receptor: functional significance in the immune system in reference to selected infections and inflammation. Ann N Y Acad Sci 1217, 83–95.
Manske JM & Hanson SE (2005) Substance‐P‐mediated immunomodulation of tumor growth in a murine model. Neuroimmunomodulation 12, 201–210.
McIlvried LA, Atherton MA, Horan NL, Goch TN & Scheff NN (2022) Sensory neurotransmitter calcitonin gene‐related peptide modulates tumor growth and lymphocyte infiltration in Oral squamous cell carcinoma. Adv Biol 6, e2200019.
Tracey KJ (2002) The inflammatory reflex. Nature 420, 853–859.
Hu J, Chen W, Shen L, Chen Z & Huang J (2022) Crosstalk between the peripheral nervous system and breast cancer influences tumor progression. Biochim Biophys Acta Rev Cancer 1877, 188828.
Reijmen E, Vannucci L, De Couck M, De Greve J & Gidron Y (2018) Therapeutic potential of the vagus nerve in cancer. Immunol Lett 202, 38–43.
Tatsuta M, Iishi H, Yamamura H, Baba M & Taniguchi H (1988) Effects of bilateral and unilateral vagotomy on gastric carcinogenesis induced by N‐methyl‐N′‐nitro‐N‐nitrosoguanidine in Wistar rats. Int J Cancer 42, 414–418.
Tatsuta M, Yamamura H, Iishi H, Ichii M, Noguchi S, Baba M & Taniguchi H (1985) Promotion by vagotomy of gastric carcinogenesis induced by N‐methyl‐N′‐nitro‐N‐nitrosoguanidine in Wistar rats. Cancer Res 45, 194–197.
Renz BW, Tanaka T, Sunagawa M, Takahashi R, Jiang Z, Macchini M, Dantes Z, Valenti G, White RA, Middelhoff MA et al. (2018) Cholinergic signaling via muscarinic receptors directly and indirectly suppresses pancreatic tumorigenesis and cancer Stemness. Cancer Discov 8, 1458–1473.
Dubeykovskaya Z, Si Y, Chen X, Worthley DL, Renz BW, Urbanska AM, Hayakawa Y, Xu T, Westphalen CB, Dubeykovskiy A et al. (2016) Neural innervation stimulates splenic TFF2 to arrest myeloid cell expansion and cancer. Nat Commun 7, 10517.
Zhang Z, Yu Q, Zhang X, Wang X, Su Y, He W, Li J, Wan H & Jing X (2021) Electroacupuncture regulates inflammatory cytokines by activating the vagus nerve to enhance antitumor immunity in mice with breast tumors. Life Sci 272, 119259.
Partecke LI, Kading A, Trung DN, Diedrich S, Sendler M, Weiss F, Kuhn JP, Mayerle J, Beyer K, von Bernstorff W et al. (2017) Subdiaphragmatic vagotomy promotes tumor growth and reduces survival via TNFalpha in a murine pancreatic cancer model. Oncotarget 8, 22501–22512.
Allen JK, Armaiz‐Pena GN, Nagaraja AS, Sadaoui NC, Ortiz T, Dood R, Ozcan M, Herder DM, Haemmerle M, Gharpure KM et al. (2018) Sustained adrenergic signaling promotes Intratumoral innervation through BDNF induction. Cancer Res 78, 3233–3242.
Globig AM, Zhao S, Roginsky J, Maltez VI, Guiza J, Avina‐Ochoa N, Heeg M, Araujo Hoffmann F, Chaudhary O, Wang J et al. (2023) The beta(1)‐adrenergic receptor links sympathetic nerves to T cell exhaustion. Nature 622, 383–392.
Isaacs JT (2013) Cancer. Prostate cancer takes nerve. Science 341, 134–135.
Zhu J, Naulaerts S, Boudhan L, Martin M, Gatto L & Van den Eynde BJ (2023) Tumour immune rejection triggered by activation of alpha2‐adrenergic receptors. Nature 618, 607–615.
Chhatar S & Lal G (2021) Role of adrenergic receptor signalling in neuroimmune communication. Curr Res Immunol 2, 202–217.
Mohammadpour H, MacDonald CR, McCarthy PL, Abrams SI & Repasky EA (2021) beta2‐adrenergic receptor signaling regulates metabolic pathways critical to myeloid‐derived suppressor cell function within the TME. Cell Rep 37, 109883.
Mohammadpour H, MacDonald CR, Qiao G, Chen M, Dong B, Hylander BL, McCarthy PL, Abrams SI & Repasky EA (2019) beta2 adrenergic receptor‐mediated signaling regulates the immunosuppressive potential of myeloid‐derived suppressor cells. J Clin Invest 129, 5537–5552.
Kokolus KM, Capitano ML, Lee CT, Eng JW, Waight JD, Hylander BL, Sexton S, Hong CC, Gordon CJ, Abrams SI et al. (2013) Baseline tumor growth and immune control in laboratory mice are significantly influenced by subthermoneutral housing temperature. Proc Natl Acad Sci USA 110, 20176–20181.
Kokolus KM, Spangler HM, Povinelli BJ, Farren MR, Lee KP & Repasky EA (2014) Stressful presentations: mild cold stress in laboratory mice influences phenotype of dendritic cells in naive and tumor‐bearing mice. Front Immunol 5, 23.
Mundy‐Bosse BL, Thornton LM, Yang HC, Andersen BL & Carson WE (2011) Psychological stress is associated with altered levels of myeloid‐derived suppressor cells in breast cancer patients. Cell Immunol 270, 80–87.
Dobrenis K, Gauthier LR, Barroca V & Magnon C (2015) Granulocyte colony‐stimulating factor off‐target effect on nerve outgrowth promotes prostate cancer development. Int J Cancer 136, 982–988.
Renz BW, Takahashi R, Tanaka T, Macchini M, Hayakawa Y, Dantes Z, Maurer HC, Chen X, Jiang Z, Westphalen CB et al. (2018) beta2 adrenergic‐Neurotrophin feedforward loop promotes pancreatic cancer. Cancer Cell 34, 863–867.
Pasquier E, Ciccolini J, Carre M, Giacometti S, Fanciullino R, Pouchy C, Montero MP, Serdjebi C, Kavallaris M & Andre N (2011) Propranolol potentiates the anti‐angiogenic effects and anti‐tumor efficacy of chemotherapy agents: implication in breast cancer treatment. Oncotarget 2, 797–809.
Thaker PH, Han LY, Kamat AA, Arevalo JM, Takahashi R, Lu C, Jennings NB, Armaiz‐Pena G, Bankson JA, Ravoori M et al. (2006) Chronic stress promotes tumor growth and angiogenesis in a mouse model of ovarian carcinoma. Nat Med 12, 939–944.
Devi S, Alexandre YO, Loi JK, Gillis R, Ghazanfari N, Creed SJ, Holz LE, Shackleford D, Mackay LK, Heath WR et al. (2021) Adrenergic regulation of the vasculature impairs leukocyte interstitial migration and suppresses immune responses. Immunity 54, 1219–1230.e7.
Goldfarb Y, Sorski L, Benish M, Levi B, Melamed R & Ben‐Eliyahu S (2011) Improving postoperative immune status and resistance to cancer metastasis: a combined perioperative approach of immunostimulation and prevention of excessive surgical stress responses. Ann Surg 253, 798–810.
Rosenne E, Sorski L, Shaashua L, Neeman E, Matzner P, Levi B & Ben‐Eliyahu S (2014) In vivo suppression of NK cell cytotoxicity by stress and surgery: glucocorticoids have a minor role compared to catecholamines and prostaglandins. Brain Behav Immun 37, 207–219.
Darvin P, Toor SM, Sasidharan Nair V & Elkord E (2018) Immune checkpoint inhibitors: recent progress and potential biomarkers. Exp Mol Med 50, 1–11.
Kamiya A, Hayama Y, Kato S, Shimomura A, Shimomura T, Irie K, Kaneko R, Yanagawa Y, Kobayashi K & Ochiya T (2019) Genetic manipulation of autonomic nerve fiber innervation and activity and its effect on breast cancer progression. Nat Neurosci 22, 1289–1305.
Mo RJ, Han ZD, Liang YK, Ye JH, Wu SL, Lin SX, Zhang YQ, Song SD, Jiang FN, Zhong WD et al. (2019) Expression of PD‐L1 in tumor‐associated nerves correlates with reduced CD8(+) tumor‐associated lymphocytes and poor prognosis in prostate cancer. Int J Cancer 144, 3099–3110.
Bucsek MJ, Qiao G, MacDonald CR, Giridharan T, Evans L, Niedzwecki B, Liu H, Kokolus KM, Eng JW, Messmer MN et al. (2017) Beta‐adrenergic signaling in mice housed at standard temperatures suppresses an effector phenotype in CD8(+) T cells and undermines checkpoint inhibitor therapy. Cancer Res 77, 5639–5651.
Jean Wrobel L, Bod L, Lengagne R, Kato M, Prevost‐Blondel A & Le Gal FA (2016) Propranolol induces a favourable shift of anti‐tumor immunity in a murine spontaneous model of melanoma. Oncotarget 7, 77825–77837.
Hiller JG, Cole SW, Crone EM, Byrne DJ, Shackleford DM, Pang JB, Henderson MA, Nightingale SS, Ho KM, Myles PS et al. (2020) Preoperative beta‐blockade with propranolol reduces biomarkers of metastasis in breast cancer: a phase II randomized trial. Clin Cancer Res 26, 1803–1811.
Sloan EK, Priceman SJ, Cox BF, Yu S, Pimentel MA, Tangkanangnukul V, Arevalo JM, Morizono K, Karanikolas BD, Wu L et al. (2010) The sympathetic nervous system induces a metastatic switch in primary breast cancer. Cancer Res 70, 7042–7052.