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HomeNatureNociceptive neurons promote gastric tumour progression via a CGRP–RAMP1 axis

Nociceptive neurons promote gastric tumour progression via a CGRP–RAMP1 axis

  • Zeng, Q. et al. Synaptic proximity enables NMDAR signalling to promote brain metastasis. Nature 573, 526–531 (2019).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Venkatesh, H. S. et al. Electrical and synaptic integration of glioma into neural circuits. Nature 573, 539–545 (2019).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Venkataramani, V. et al. Glutamatergic synaptic input to glioma cells drives brain tumour progression. Nature 573, 532–538 (2019).

    Article 
    ADS 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Hanahan, D. & Monje, M. Cancer hallmarks intersect with neuroscience in the tumor microenvironment. Cancer Cell 41, 573–580 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Venkataramani, V. et al. Glioblastoma hijacks neuronal mechanisms for brain invasion. Cell 185, 2899–2917 (2022).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Krishna, S. et al. Glioblastoma remodelling of human neural circuits decreases survival. Nature 617, 599–607 (2023).

  • Hyman, S. E. Neurotransmitters. Curr. Biol. 15, R154–R158 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Balood, M. et al. Nociceptor neurons affect cancer immunosurveillance. Nature 611, 405–412 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, Y. et al. Cancer cells co-opt nociceptive nerves to thrive in nutrient-poor environments and upon nutrient-starvation therapies. Cell Metab. 34, 1999–2017.e10 (2022).

  • Reavis, H. D., Chen, H. I. & Drapkin, R. Tumor innervation: cancer has some nerve. Trends Cancer 6, 1059–1067 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhao, C. M. et al. Denervation suppresses gastric tumorigenesis. Sci. Transl. Med. 6, 250ra115 (2014).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Berthoud, H. R. & Neuhuber, W. L. Functional and chemical anatomy of the afferent vagal system. Auton. Neurosci. 85, 1–17 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hayakawa, Y. et al. Nerve growth factor promotes gastric tumorigenesis through aberrant cholinergic signaling. Cancer Cell 31, 21–34 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chang, W. et al. Hormonal suppression of stem cells inhibits symmetric cell division and gastric tumorigenesis. Cell Stem Cell 26, 739–754 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Till, J. E. et al. Oncogenic KRAS and p53 loss drive gastric tumorigenesis in mice that can be attenuated by E-cadherin expression. Cancer Res. 77, 5349–5359 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Ma, L., Lei, L., Eng, S. R., Turner, E. & Parada, L. F. Brn3a regulation of TrkA/NGF receptor expression in developing sensory neurons. Development 130, 3525–3534 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lee, S. et al. NGF-TrkA signaling dictates neural ingrowth and aberrant osteochondral differentiation after soft tissue trauma. Nat. Commun. 12, 4939 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Ji, R. R., Samad, T. A., Jin, S. X., Schmoll, R. & Woolf, C. J. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36, 57–68 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hayakawa, Y. et al. Mist1 expressing gastric stem cells maintain the normal and neoplastic gastric epithelium and are supported by a perivascular stem cell niche. Cancer Cell 28, 800–814 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Ahluwalia, A. et al. Reduced NGF in gastric endothelial cells is one of the main causes of impaired angiogenesis in aging gastric mucosa. Cell. Mol. Gastroenterol. Hepatol. 6, 199–213 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Callaway, E. M. & Luo, L. Monosynaptic circuit tracing with glycoprotein-deleted rabies viruses. J. Neurosci. 35, 8979–8985 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Russell, F. A., King, R., Smillie, S. J., Kodji, X. & Brain, S. D. Calcitonin gene-related peptide: physiology and pathophysiology. Physiol. Rev. 94, 1099–1142 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kim, Y. J. & Granstein, R. D. Roles of calcitonin gene-related peptide in the skin, and other physiological and pathophysiological functions. Brain Behav. Immun. Health 18, 100361 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yang, D. et al. Nociceptor neurons direct goblet cells via a CGRP-RAMP1 axis to drive mucus production and gut barrier protection. Cell 185, 4190–4205 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Horie, S., Michael, G. J. & Priestley, J. V. Co-localization of TRPV1-expressing nerve fibers with calcitonin-gene-related peptide and substance P in fundus of rat stomach. Inflammopharmacology 13, 127–137 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Okabe, S. & Amagase, K. An overview of acetic acid ulcer models-the history and state of the art of peptic ulcer research. Biol. Pharm. Bull. 28, 1321–1341 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lai, N. Y. et al. Gut-innervating nociceptor neurons regulate peyer’s patch microfold cells and SFB levels to mediate Salmonella host defense. Cell 180, 33–49 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Le, T. T. et al. Sensory nerves enhance triple-negative breast cancer invasion and metastasis via the axon guidance molecule PlexinB3. npj Breast Cancer 8, 116 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Filliol, A. et al. Opposing roles of hepatic stellate cell subpopulations in hepatocarcinogenesis. Nature 610, 356–365 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Carr, R. & Frings, S. Neuropeptides in sensory signal processing. Cell Tissue Res. 375, 217–225 (2019).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Bocchi, R., Masserdotti, G. & Gotz, M. Direct neuronal reprogramming: fast forward from new concepts toward therapeutic approaches. Neuron 110, 366–393 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Vermeiren, S., Bellefroid, E. J. & Desiderio, S. Vertebrate sensory ganglia: common and divergent features of the transcriptional programs generating their functional specialization. Front. Cell Dev. Biol. 8, 587699 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tomlinson, R. E. et al. NGF-TrkA signaling in sensory nerves is required for skeletal adaptation to mechanical loads in mice. Proc. Natl Acad. Sci. USA 114, E3632–E3641 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Umoh, N. A. et al. Calcitonin gene-related peptide regulates cardiomyocyte survival through regulation of oxidative stress by PI3K/Akt and MAPK signaling pathways. Ann. Clin. Exp. Hypertens. 2, 1007 (2014).

    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Venkatesh, H. S. et al. Neuronal activity promotes glioma growth through neuroligin-3 secretion. Cell 161, 803–816 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Peterson, S. C. et al. Basal cell carcinoma preferentially arises from stem cells within hair follicle and mechanosensory niches. Cell Stem Cell 16, 400–412 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 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).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Restaino, A. C. et al. Functional neuronal circuits promote disease progression in cancer. Sci. Adv. 9, eade4443 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Zhong, F., Christianson, J. A., Davis, B. M. & Bielefeldt, K. Dichotomizing axons in spinal and vagal afferents of the mouse stomach. Dig. Dis. Sci. 53, 194–203 (2008).

    Article 
    PubMed 

    Google Scholar
     

  • Lobikin, M., Chernet, B., Lobo, D. & Levin, M. Resting potential, oncogene-induced tumorigenesis, and metastasis: the bioelectric basis of cancer in vivo. Phys. Biol. 9, 065002 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yang, M. & Brackenbury, W. J. Membrane potential and cancer progression. Front. Physiol. 4, 185 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Lukyanetz, E. A. Different secretory vesicles can be involved in depolarization-evoked exocytosis. Biochem. Biophys. Res. Commun. 288, 844–848 (2001).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Bohorquez, D. V. et al. Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells. J. Clin. Invest. 125, 782–786 (2015).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Zhang, W. et al. Gut-innervating nociceptors regulate the intestinal microbiota to promote tissue protection. Cell 185, 4170–4189 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Gao, X. et al. Nociceptive nerves regulate haematopoietic stem cell mobilization. Nature 589, 591–596 (2021).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • 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).

    Article 

    Google Scholar
     

  • Edvinsson, L., Haanes, K. A., Warfvinge, K. & Krause, D. N. CGRP as the target of new migraine therapies—successful translation from bench to clinic. Nat. Rev. Neurol. 14, 338–350 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Elser, H. et al. Cancer risk in patients with migraine: a population-based cohort study in Denmark. Headache 62, 57–64 (2022).

    Article 
    PubMed 
    MATH 

    Google Scholar
     

  • Hayakawa, Y. et al. BHLHA15-positive secretory precursor cells can give rise to tumors in intestine and colon in mice. Gastroenterology 156, 1066–1081 (2019).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Zhan, J., Komal, R., Keenan, W. T., Hattar, S. & Fernandez, D. C. Non-invasive strategies for chronic manipulation of DREADD-controlled neuronal activity. J. Vis. Exp. https://doi.org/10.3791/59439 (2019).

  • de Sousae Melo, F. et al. A distinct role for Lgr5+ stem cells in primary and metastatic colon cancer. Nature 543, 676–680 (2017).

    Article 
    ADS 

    Google Scholar
     

  • Ayer, A. et al. Techniques of sleeve gastrectomy and modified Roux-en-Y gastric bypass in mice. J. Vis. Exp. https://doi.org/10.3791/54905 (2017).

  • Kaelberer, M. M. et al. A gut-brain neural circuit for nutrient sensory transduction. Science 361, eaat5236 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wolf, F. A. et al. SCANPY: large-scale single-cell gene expression data analysis. Genome Biol. 19, 15 (2018).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

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