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Abstract

The nervous system is intimately involved in physiological processes from development and growth to tissue homeostasis and repair throughout the body. It logically follows that the nervous system has the potential to play analogous roles in the context of cancer. Progress toward understanding the crucial role of the nervous system in cancer has accelerated in recent years, but much remains to be learned. Here, we highlight rapidly evolving concepts in this burgeoning research space and consider next steps toward understanding and therapeutically targeting the neural regulation of cancer.

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2020-03-04
2024-12-13
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Literature Cited

  1. Achrol AS, Rennert RC, Anders C, Soffietti R, Ahluwalia MS et al. 2019. Brain metastases. Nat. Rev. Dis. Primers 5:15
    [Google Scholar]
  2. Aihara T, Fujishita T, Kanatani K, Furutani K, Nakamura E et al. 2003. Impaired gastric secretion and lack of trophic responses to hypergastrinemia in M3 muscarinic receptor knockout mice. Gastroenterology 125:61774–84
    [Google Scholar]
  3. Ayala G, Liebig C, Wilks JA, Albo D, Berger DH 2009. Perineural invasion in cancer. Cancer 115:153379–91
    [Google Scholar]
  4. Ayala GE, Wheeler TM, Shine HD, Schmelz M, Frolov A et al. 2001. In vitro dorsal root ganglia and human prostate cell line interaction: redefining perineural invasion in prostate cancer. Prostate 49:3213–23
    [Google Scholar]
  5. Banasr M, Hery M, Printemps R, Daszuta A 2004. Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology 29:3450–60
    [Google Scholar]
  6. Barami K, Sloan AE, Rojiani A, Schell MJ, Staller A, Brem S 2009. Relationship of gliomas to the ventricular walls. J. Clin. Neurosci. 16:2195–201
    [Google Scholar]
  7. Barbieri A, Bimonte S, Palma G, Luciano A, Rea D et al. 2015. The stress hormone norepinephrine increases migration of prostate cancer cells in vitro and in vivo. Int. J. Oncol. 47:2527–34
    [Google Scholar]
  8. Barres BA, Raff MC. 1993. Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361:258–60
    [Google Scholar]
  9. Batsakis JG. 1985. Nerves and neurotropic carcinomas. Ann. Otol. Rhinol. Laryngol. 94:426–27
    [Google Scholar]
  10. Batlle E, Clevers H. 2017. Cancer stem cells revisited. Nat. Med. 23:101124–34
    [Google Scholar]
  11. Bergles DE, Richardson WD. 2015. Oligodendrocyte development and plasticity. Cold Spring Harb. Perspect. Biol. 8:2a020453
    [Google Scholar]
  12. Bergles DE, Roberts JD, Somogyi P, Jahr CE 2000. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405:6783187–91
    [Google Scholar]
  13. Bittman K, Owens DF, Kriegstein AR, LoTurco JJ 1997. Cell coupling and uncoupling in the ventricular zone of developing neocortex. J. Neurosci. 17:187037–44
    [Google Scholar]
  14. Blanchart A, Fernando R, Häring M, Assaife-Lopes N, Romanov RA et al. 2017. Endogenous GABAA receptor activity suppresses glioma growth. Oncogene 36:6777–86
    [Google Scholar]
  15. Boilly B, Faulkner S, Jobling P, Hondermarck H 2017. Nerve dependence: from regeneration to cancer. Cancer Cell 31:33432–54
    [Google Scholar]
  16. Borniger JC, Walker WH 2nd, Surbhi, Emmer KM, Zhang N et al. 2018. A role for hypocretin/orexin in metabolic and sleep abnormalities in a mouse model of non-metastatic breast cancer. Cell Metab 28:1118–29.e5
    [Google Scholar]
  17. Brownell I, Guevara E, Bai CB, Loomis CA, Joyner AL 2011. Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell 8:5552–65
    [Google Scholar]
  18. Buckingham SC, Campbell SL, Haas BR, Montana V, Robel S et al. 2011. Glutamate release by primary brain tumors induces epileptic activity. Nat. Med. 17:101269–74
    [Google Scholar]
  19. Campbell SL, Buckingham SC, Sontheimer H 2012. Human glioma cells induce hyperexcitability in cortical networks. Epilepsia 53:81360–70
    [Google Scholar]
  20. Campbell SL, Robel S, Cuddapah VA, Robert S, Buckingham SC et al. 2015. GABAergic disinhibition and impaired KCC2 cotransporter activity underlie tumor-associated epilepsy. Glia 63:123–36
    [Google Scholar]
  21. Canudas AM. 2004. PHCCC, a specific enhancer of type 4 metabotropic glutamate receptors, reduces proliferation and promotes differentiation of cerebellar granule cell neuroprecursors. J. Neurosci. 24:4610343–52
    [Google Scholar]
  22. Caretti V, Bugiani M, Freret M, Schellen P, Jansen M et al. 2014. Subventricular spread of diffuse intrinsic pontine glioma. Acta Neuropathol 128:4605–7
    [Google Scholar]
  23. Carter RL, Tanner NSB, Clifford P, Shaw HJ 1979. Perineural spread in squamous cell carcinomas of the head and neck: a clinicopathological study. Clin. Otolaryngol. Allied Sci. 4:4271–81
    [Google Scholar]
  24. Cassiman D, Libbrecht L, Sinelli N, Desmet V, Denef C, Roskams T 2002. The vagal nerve stimulates activation of the hepatic progenitor cell compartment via muscarinic acetylcholine receptor type 3. Am. J. Pathol. 161:2521–30
    [Google Scholar]
  25. Ceyhan GO, Bergmann F, Kadihasanoglu M, Altintas B, Demir IE et al. 2009. Pancreatic neuropathy and neuropathic pain—a comprehensive pathomorphological study of 546 cases. Gastroenterology 136:1177–86.e1
    [Google Scholar]
  26. Chaichana KL, McGirt MJ, Frazier J, Attenello F, Guerrero-Cazares H, Quinones-Hinojosa A 2008. Relationship of glioblastoma multiforme to the lateral ventricles predicts survival following tumor resection. J. Neurooncol. 89:2219–24
    [Google Scholar]
  27. Chavan SS, Pavlov VA, Tracey KJ 2017. Mechanisms and therapeutic relevance of neuro-immune communication. Immunity 46:6927–42
    [Google Scholar]
  28. Chen Q, Boire A, Jin X, Valiente M, Er EE et al. 2016. Carcinoma-astrocyte gap junctions promote brain metastasis by cGAMP transfer. Nature 533:7604493–98
    [Google Scholar]
  29. Cocco E, Scaltriti M, Drilon A 2018. NTRK fusion-positive cancers and TRK inhibitor therapy. Nat. Rev. Clin. Oncol. 15:12731–47
    [Google Scholar]
  30. Cohen S, Levi-Montalcini R, Hamburger V 1954. A nerve growth–stimulating factor isolated from sarcomas 37 and 180. PNAS 40:101014–18
    [Google Scholar]
  31. Cole SW, Nagaraja AS, Lutgendorf SK, Green PA, Sood AK 2015. Sympathetic nervous system regulation of the tumour microenvironment. Nat. Rev. Cancer 15:9563–72
    [Google Scholar]
  32. Corlew R, Bosma MM, Moody WJ 2004. Spontaneous, synchronous electrical activity in neonatal mouse cortical neurones. J. Physiol. 560:2377–90
    [Google Scholar]
  33. Cui B, Kelley KW, Liu Q, Cui B, Luo Y et al. 2019. Stress-induced epinephrine enhances lactate dehydrogenase A and promotes breast cancer. J. Clin. Investig. 129:31030–46
    [Google Scholar]
  34. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC 2004. Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42:535–52
    [Google Scholar]
  35. Dolma S, Selvadurai HJ, Lan X, Lee L, Kushida M et al. 2016. Inhibition of dopamine receptor D4 impedes autophagic flux, proliferation, and survival of glioblastoma stem cells. Cancer Cell 29:6859–73
    [Google Scholar]
  36. Emmerson E, May AJ, Berthoin L, Cruz‐Pacheco N, Nathan S et al. 2018. Salivary glands regenerate after radiation injury through SOX2‐mediated secretory cell replacement. EMBO Mol. Med. 10:3e8051
    [Google Scholar]
  37. Filbin MG, Tirosh I, Hovestadt V, Shaw ML, Escalante LE et al. 2018. Developmental and oncogenic programs in H3K27M gliomas dissected by single-cell RNA-seq. Science 360:6386331–35
    [Google Scholar]
  38. Geraghty AC, Gibson EM, Ghanem RA, Greene JJ, Ocampo A et al. 2019. Loss of adaptive myelination contributes to methotrexate chemotherapy-related cognitive impairment. Neuron 103:2250–65.e8
    [Google Scholar]
  39. Gibson EM, Purger D, Mount CW, Goldstein AK, Lin GL et al. 2014. Oligodendrogenesis and adaptive myelination in the mammalian brain. Science 344:487–99
    [Google Scholar]
  40. Gillespie S, Monje M. 2018. An active role for neurons in glioma progression: making sense of Scherer's structures. Neuro-Oncology 20:101292–99
    [Google Scholar]
  41. Golomb E, Kruglikova A, Dvir D, Parnes N, Abramovici A 1998. Induction of atypical prostatic hyperplasia in rats by sympathomimetic stimulation. Prostate 34:3214–21
    [Google Scholar]
  42. Gross ER, Gershon MD, Margolis KG, Gertsberg ZV, Cowles RA 2012. Neuronal serotonin regulates growth of the intestinal mucosa in mice. Gastroenterology 143:2408–17.e2
    [Google Scholar]
  43. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144:646–74
    [Google Scholar]
  44. Hassan S, Karpova Y, Baiz D, Yancey D, Pullikuth A, Kulik G 2013. Behavioral stress accelerates prostate cancer development in mice. J. Clin. Investig. 123:2874–86
    [Google Scholar]
  45. Hayakawa Y, Sakitani K, Konishi M, Asfaha S, Niikura R et al. 2017. Nerve growth factor promotes gastric tumorigenesis through aberrant cholinergic signaling. Cancer Cell 31:21–34
    [Google Scholar]
  46. Hill RA, Li AM, Grutzendler J 2018. Lifelong cortical myelin plasticity and age-related degeneration in the live mammalian brain. Nat. Neurosci. 21:5683–95
    [Google Scholar]
  47. Hughes EG, Kang SH, Fukaya M, Bergles DE 2013. Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat. Neurosci. 16:668–76
    [Google Scholar]
  48. Hughes EG, Orthmann-Murphy JL, Langseth AJ, Bergles DE 2018. Myelin remodeling through experience-dependent oligodendrogenesis in the adult somatosensory cortex. Nat. Neurosci. 21:5696–706
    [Google Scholar]
  49. Imayoshi I, Kageyama R. 2011. The role of notch signaling in adult neurogenesis. Mol. Neurobiol. 44:17–12
    [Google Scholar]
  50. Ishiuchi S, Tsuzuki K, Yoshida Y, Yamada N, Hagimura N et al. 2002. Blockage of Ca2+-permeable AMPA receptors suppresses migration and induces apoptosis in human glioblastoma cells. Nat. Med. 8:9971–78
    [Google Scholar]
  51. Ishiuchi S, Yoshida Y, Sugawara K, Aihara M, Ohtani T et al. 2007. Ca2+-permeable AMPA receptors regulate growth of human glioblastoma via Akt activation. J. Neurosci. 27:307987–8001
    [Google Scholar]
  52. Kaneko T, Nakao A, Inoue S, Nomoto IS, Nagasaka T, Nakashima N 1996. Extrapancreatic nerve plexus invasion by carcinoma of the head of the pancreas. Int. J. Pancreatol. 19:11–7
    [Google Scholar]
  53. Kim-Fuchs C, Le CP, Pimentel MA, Shackleford D, Ferrari D et al. 2014. Chronic stress accelerates pancreatic cancer growth and invasion: a critical role for beta-adrenergic signaling in the pancreatic microenvironment. Brain. Behav. Immun. 40:40–47
    [Google Scholar]
  54. Knox SM. 2010. Parasympathetic innvervation maintains epithelial progenitor cells during salivary organogenesis. Science 329:59991645–47
    [Google Scholar]
  55. Kougioumtzidou E, Shimizu T, Hamilton NB, Tohyama K, Sprengel R et al. 2017. Signalling through AMPA receptors on oligodendrocyte precursors promotes myelination by enhancing oligodendrocyte survival. eLife 6:e28080
    [Google Scholar]
  56. Kreso A, Dick JE. 2014. Evolution of the cancer stem cell model. Cell Stem Cell 14:3275–91
    [Google Scholar]
  57. Labrakakis C, Patt S, Hartmann J, Kettenmann H 1998. Functional GABAA receptors on human glioma cells. Eur. J. Neurosci. 10:1231–38
    [Google Scholar]
  58. Lan X, Jörg DJ, Cavalli FMG, Richards LM, Nguyen LV et al. 2017. Fate mapping of human glioblastoma reveals an invariant stem cell hierarchy. Nature 549:7671227–32
    [Google Scholar]
  59. Lathia JD, Mack SC, Mulkearns-Hubert EE 2015. Tumor stem cells in glioblastoma. Genes Dev 29:121203–17
    [Google Scholar]
  60. Lawn S, Krishna N, Pisklakova A, Qu X, Fenstermacher DA et al. 2015. Neurotrophin signaling via TrkB and TrkC receptors promotes the growth of brain tumor-initiating cells. J. Biol. Chem. 290:63814–24
    [Google Scholar]
  61. Lee JH, Lee JE, Kahng JY, Kim SH, Park JS et al. 2018. Human glioblastoma arises from subventricular zone cells with low-level driver mutations. Nature 560:7717243–47
    [Google Scholar]
  62. Liebig C, Ayala G, Wilks J, Verstovsek G, Liu H et al. 2009. Perineural invasion is an independent predictor of outcome in colorectal cancer. J. Clin. Oncol. 27:315131–37
    [Google Scholar]
  63. Lin C-CJ, Yu K, Hatcher A, Huang T-W, Lee HK et al. 2017. Identification of diverse astrocyte populations and their malignant analogs. Nat. Neurosci. 20:3396–405
    [Google Scholar]
  64. Lin SC, Bergles DE. 2004. Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nat. Neurosci. 7:124–32
    [Google Scholar]
  65. Liu C, Sage JC, Miller MR, Verhaak RGW, Hippenmeyer S et al. 2011. Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell 146:209–21
    [Google Scholar]
  66. Liu X, Wang Q, Haydar TF, Bordey A 2005. Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat. Neurosci. 8:91179–87
    [Google Scholar]
  67. Llaguno S, Sun D, Pedraza AM, Vera E, Wang Z et al. 2019. Cell-of-origin susceptibility to glioblastoma formation declines with neural lineage restriction. Nat. Neurosci. 22:4545–55
    [Google Scholar]
  68. Lois C, Alvarez-Buylla A. 1994. Long-distance neuronal migration in the adult mammalian brain. Science 264:51621145–48
    [Google Scholar]
  69. LoTurco J, Blanton M, Kriegstein A 1991. Initial expression and endogenous activation of NMDA channels in early neocortical development. J. Neurosci. 11:3792–99
    [Google Scholar]
  70. Lundgaard I, Luzhynskaya A, Stockley JH, Wang Z, Evans KA et al. 2013. Neuregulin and BDNF induce a switch to NMDA receptor-dependent myelination by oligodendrocytes. PLOS Biol 11:12e1001743
    [Google Scholar]
  71. Lundgren O, Jodal M, Jansson M, Ryberg AT, Svensson L 2011. Intestinal epithelial stem/progenitor cells are controlled by mucosal afferent nerves. PLOS ONE 6:2e16295
    [Google Scholar]
  72. Lyons SA, Chung WJ, Weaver AK, Ogunrinu T, Sontheimer H 2007. Autocrine glutamate signaling promotes glioma cell invasion. Cancer Res 67:199463–71
    [Google Scholar]
  73. Mack SC, Hubert CG, Miller TE, Taylor MD, Rich JN 2015. An epigenetic gateway to brain tumor cell identity. Nat. Neurosci. 19:110–19
    [Google Scholar]
  74. Magnon C, Hall SJ, Lin J, Xue X, Gerber L et al. 2013. Autonomic nerve development cancer progression. Science 341:61421236361
    [Google Scholar]
  75. Mahe C, Bernhard M, Bobirnac I, Keser C, Loetscher E et al. 2004. Functional expression of the serotonin 5-HT7 receptor in human glioblastoma cell lines. Br. J. Pharmacol. 143:404–10
    [Google Scholar]
  76. Marins M, Xavier ALR, Viana NB, Fortes FSA, Fróes MM, Menezes JRL 2009. Gap junctions are involved in cell migration in the early postnatal subventricular zone. Dev. Neurobiol. 69:11715–30
    [Google Scholar]
  77. Martincorena I, McLaren S, Tubio JM, Campbell PJ, Van Loo P et al. 2015. High burden and pervasive positive selection of somatic mutations in normal human skin. Science 348:6237880–86
    [Google Scholar]
  78. Maru N, Ohori M, Kattan MW, Scardino PT, Wheeler TM 2001. Prognostic significance of the diameter of perineural invasion in radical prostatectomy specimens. Hum. Pathol. 32:8828–33
    [Google Scholar]
  79. McKenzie IA, Ohayon D, Li H, De Faria JP, Emery B et al. 2014. Motor skill learning requires active central myelination. Science 346:6207318–22
    [Google Scholar]
  80. McVary KT, Razzaq A, Lee C, Venegas MF, Rademaker A, McKenna KE 1994. Growth of the rat prostate gland is facilitated by the autonomic nervous system. Biol. Reprod. 51:199–107
    [Google Scholar]
  81. Mitew S, Gobius I, Fenlon LR, McDougall S, Hawkes D et al. 2018. Pharmacogenetic stimulation of neuronal activity increases myelination in an axon-specific manner. Nat. Commun. 9:306
    [Google Scholar]
  82. Mitsunaga S, Hasebe T, Kinoshita T, Konishi M, Takahashi S et al. 2007. Detail histologic analysis of nerve plexus invasion in invasive ductal carcinoma of the pancreas and its prognostic impact. Am. J. Surg. Pathol. 31:111636–44
    [Google Scholar]
  83. Monje M, Mitra SS, Freret ME, Raveh TB, Kim J et al. 2011. Hedgehog-responsive candidate cell of origin for diffuse intrinsic pontine glioma. PNAS 108:114453–58
    [Google Scholar]
  84. Mount CW, Monje M. 2017. Wrapped to adapt: experience-dependent myelination. Neuron 95:4743–56
    [Google Scholar]
  85. Nagaraja S, Vitanza NA, Woo PJ, Taylor KR, Liu F et al. 2017. Transcriptional dependencies in diffuse intrinsic pontine glioma. Cancer Cell 31:5635–52.e6
    [Google Scholar]
  86. Nedvetsky PI, Emmerson E, Finley JK, Ettinger A, Cruz-Pacheco N et al. 2014. Parasympathetic innervation regulates tubulogenesis in the developing salivary gland. Dev. Cell 30:4449–62
    [Google Scholar]
  87. Neftel C, Laffy J, Filbin MG, Hara T, Shore ME et al. 2019. An integrative model of cellular states, plasticity, and genetics for glioblastoma. Cell 178:4835–49.e21
    [Google Scholar]
  88. O'Brien CJ, Carter RL, Soo K‐C, Barr LC, Hamlyn PJ, Shaw HJ 1986. Invasion of the mandible by squamous carcinomas of the oral cavity and oropharynx. Head Neck Surg 8:4247–56
    [Google Scholar]
  89. O'Keeffe GC, Tyers P, Aarsland D, Dalley JW, Barker RA, Caldwell MA 2009. Dopamine-induced proliferation of adult neural precursor cells in the mammalian subventricular zone is mediated through EGF. PNAS 106:218754–59
    [Google Scholar]
  90. Olar A, He D, Florentin D, Ding Y, Wheeler T, Ayala G 2014. Biological correlates of prostate cancer perineural invasion diameter. Hum. Pathol. 45:71365–69
    [Google Scholar]
  91. Osswald M, Jung E, Sahm F, Solecki G, Venkataramani V et al. 2015. Brain tumour cells interconnect to a functional and resistant network. Nature 528:758093–98
    [Google Scholar]
  92. Paez-Gonzalez P, Asrican B, Rodriguez E, Kuo CT 2014. Identification of distinct ChAT+ neurons and activity-dependent control of postnatal SVZ neurogenesis. Nat. Neurosci. 17:7934–42
    [Google Scholar]
  93. Palm D, Lang K, Niggemann B, Drell IV TL, Masur K et al. 2006. The norepinephrine-driven metastasis development of PC-3 human prostate cancer cells in BALB/c nude mice is inhibited by β-blockers. Int. J. Cancer 118:112744–49
    [Google Scholar]
  94. Partecke LI, Speerforck S, Käding A, Seubert F, Kühn S et al. 2016. Chronic stress increases experimental pancreatic cancer growth, reduces survival and can be antagonised by beta-adrenergic receptor blockade. Pancreatology 16:3423–33
    [Google Scholar]
  95. Patel AP, Tirosh I, Trombetta JJ, Shalek AK, Gillespie SM et al. 2014. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 344:61901396–401
    [Google Scholar]
  96. Peterson SC, Eberl M, Vagnozzi AN, Belkadi A, Veniaminova NA et al. 2015. Basal cell carcinoma preferentially arises from stem cells within hair follicle and mechanosensory niches. Cell Stem Cell 16:4400–12
    [Google Scholar]
  97. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH et al. 2006. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9:157–73
    [Google Scholar]
  98. Platel JC, Dave KA, Gordon V, Lacar B, Rubio ME, Bordey A 2010. NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network. Neuron 65:6859–72
    [Google Scholar]
  99. Pundavela J, Demont Y, Jobling P, Lincz LF, Roselli S et al. 2014. ProNGF correlates with Gleason score and is a potential driver of nerve infiltration in prostate cancer. Am. J. Pathol. 184:123156–62
    [Google Scholar]
  100. Qin EY, Cooper DD, Abbott KL, Lennon J, Nagaraja S et al. 2017. Neural precursor-derived pleiotrophin mediates subventricular zone invasion by glioma. Cell 170:5845–59.e19
    [Google Scholar]
  101. Renz BW, Takahashi R, Tanaka T, Iuga AC, Olive KP, Wang TC 2018. β2 adrenergic-neurotrophin feedforward loop promotes pancreatic cancer. Cancer Cell 33:175–90.e7
    [Google Scholar]
  102. Rushing G, Ihrie RA. 2016. Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone. Front. Biol. 11:4261–84
    [Google Scholar]
  103. Saloman JL, Albers KM, Li D, Hartman DJ, Crawford HC et al. 2016. Ablation of sensory neurons in a genetic model of pancreatic ductal adenocarcinoma slows initiation and progression of cancer. PNAS 113:113078–83
    [Google Scholar]
  104. Sastry KSR, Karpova Y, Prokopovich S, Smith AJ, Essau B et al. 2007. Epinephrine protects cancer cells from apoptosis via activation of cAMP-dependent protein kinase and BAD phosphorylation. J. Biol. Chem. 282:1914094–100
    [Google Scholar]
  105. Stopczynski RE, Normolle DP, Hartman DJ, Ying H, DeBerry JJ et al. 2014. Neuroplastic changes occur early in the development of pancreatic ductal adenocarcinoma. Cancer Res 74:61718–27
    [Google Scholar]
  106. Suvà ML, Rheinbay E, Gillespie SM, Patel AP, Wakimoto H et al. 2014. Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells. Cell 157:3580–94
    [Google Scholar]
  107. Takahashi T, Ishikura H, Motohara T, Okushiba SI, Dohke M, Katoh H 1997. Perineural invasion by ductal adenocarcinoma of the pancreas. J. Surg. Oncol. 65:3164–70
    [Google Scholar]
  108. Takano T, Lin JHC, Arcuino G, Gao Q, Yang J, Nedergaard M 2001. Glutamate release promotes growth of malignant gliomas. Nat. Med. 7:91010–15
    [Google Scholar]
  109. Thaker PH, Han LY, Kamat AA, Arevalo JM, Takahashi R et al. 2006. Chronic stress promotes tumor growth and angiogenesis in a mouse model of ovarian carcinoma. Nat. Med. 12:8939–44
    [Google Scholar]
  110. Tirosh I, Venteicher AS, Hebert C, Escalante LE, Patel AP et al. 2016. Single-cell RNA-seq supports a developmental hierarchy in human oligodendroglioma. Nature 539:309–13
    [Google Scholar]
  111. Tripathi RB, Jackiewicz M, McKenzie IA, Kougioumtzidou E, Grist M, Richardson WD 2017. Remarkable stability of myelinating oligodendrocytes in mice. Cell Rep 21:2316–23
    [Google Scholar]
  112. Ullrich NJ, Pomeroy SL, Kapur K, Manley PE, Goumnerova LC, Loddenkemper T 2015. Incidence, risk factors, and longitudinal outcome of seizures in long-term survivors of pediatric brain tumors. Epilepsia 56:101599–604
    [Google Scholar]
  113. Ulrich-Lai YM, Herman JP. 2009. Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 10:6397–409
    [Google Scholar]
  114. Van Kampen JM, Hagg T, Robertson HA 2004. Induction of neurogenesis in the adult rat subventricular zone and neostriatum following dopamine D3 receptor stimulation. Eur. J. Neurosci. 19:92377–87
    [Google Scholar]
  115. Venkataramani V, Tanev DI, Strahle C, Studier-Fischer A, Fankhauser L et al. 2019. Glutamatergic synaptic input to glioma cells drives brain tumour progression. Nature 573:532–38
    [Google Scholar]
  116. Venkatesh HS, Johung TB, Caretti V, Noll A, Tang Y et al. 2015. Neuronal activity promotes glioma growth through neuroligin-3 secretion. Cell 161:4803–16
    [Google Scholar]
  117. Venkatesh HS, Morishita W, Geraghty AC, Silverbush D, Gillespie SM et al. 2019. Electrical and synaptic integration of glioma into neural circuits. Nature 573:539–45
    [Google Scholar]
  118. Venkatesh HS, Tam LT, Woo PJ, Lennon J, Nagaraja S et al. 2017. Targeting neuronal activity-regulated neuroligin-3 dependency in high-grade glioma. Nature 549:7673533–37
    [Google Scholar]
  119. Venteicher AS, Tirosh I, Hebert C, Yizhak K, Neftel C et al. 2017. Decoupling genetics, lineages, and microenvironment in IDH-mutant gliomas by single-cell RNA-seq. Science 355:6332eaai8478
    [Google Scholar]
  120. Verhaak RGW, Hoadley KA, Purdom E, Wang V, Qi Y et al. 2010. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17:198–110
    [Google Scholar]
  121. Villers A. 1989. The role of perineural space invasion in the local spread of prostatic adenocarcinoma. J. Urol. 142:3763–68
    [Google Scholar]
  122. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA Jr., Kinzler KW 2013. Cancer genome landscapes. Science 339:61271546–58
    [Google Scholar]
  123. Walker AK, Martelli D, Ziegler AI, Lambert GW, Phillips SE et al. 2019. Circulating epinephrine is not required for chronic stress to enhance metastasis. Psychoneuroendocrinology 99:191–95
    [Google Scholar]
  124. Wallace VA. 1999. Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr. Biol. 9:8445–48
    [Google Scholar]
  125. Weissman TA, Riquelme PA, Ivic L, Flint AC, Kriegstein AR 2004. Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43:5647–61
    [Google Scholar]
  126. Wong ROL. 1995. Effects of glutamate and its analogs on intracellular calcium levels in the developing retina. Vis. Neurosci. 12:5907–17
    [Google Scholar]
  127. Xiao Y, Thoresen DT, Williams JS, Wang C, Perna J et al. 2015. Neural Hedgehog signaling maintains stem cell renewal in the sensory touch dome epithelium. PNAS 112:237195–200
    [Google Scholar]
  128. Ye Z, Sontheimer H. 1999. Glioma cells release excitotoxic concentrations of glutamate. Cancer Res 59:4383–91
    [Google Scholar]
  129. Zahalka AH, Arnal-Estapé A, Maryanovich M, Nakahara F, Cruz CD et al. 2017. Adrenergic nerves activate an angio-metabolic switch in prostate cancer. Science 326:321–26
    [Google Scholar]
  130. Zeng Q, Michael IP, Zhang P, Saghafinia S, Knott G et al. 2019. Synaptic proximity enables NMDAR signalling to promote brain metastasis. Nature 573:7775526–31
    [Google Scholar]
  131. Zhang Z, Hu F, Liu Y, Ma B, Chen X et al. 2016. Activation of type 5 metabotropic glutamate receptor promotes the proliferation of rat retinal progenitor cell via activation of the PI-3-K and MAPK signaling pathways. Neuroscience 322:138–51
    [Google Scholar]
  132. Zhao CM, Hayakawa Y, Kodama Y, Muthupalani S, Westphalen CB et al. 2014. Denervation suppresses gastric tumorigenesis. Sci. Transl. Med. 6:250250ra115
    [Google Scholar]
  133. Zong H, Parada LF, Baker SJ 2015. Cell of origin for malignant gliomas and its implication in therapeutic development. Cold Spring Harb. Perspect. Biol. 7:5a020610
    [Google Scholar]
  134. Zonouzi M, Scafidi J, Li P, McEllin B, Edwards J et al. 2015. GABAergic regulation of cerebellar NG2 cell development is altered in perinatal white matter injury. Nat. Neurosci. 18:5674–82
    [Google Scholar]
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