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The relationship between the tumor and its innervation: historical, methodical, morphological, and functional assessments – A minireview


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Adler I, Sittenfield MJ. Preliminary note on the possible effects of the nervous system upon the growth and development of tumors. J Cancer Res 2, 239–244, 1917.Search in Google Scholar

Amit M, Takahashi H, Dragomir MP, Lindemann A, Gleber-Netto FO, Pickering CR, Anfossi S, Osman AA, Cai Y, Wang R, Knutsen E, Shimizu M, Ivan C, Rao X, Wang J, Silverman DA, Tam S, Zhao M, Caulin C, Zinger A, Tasciotti E, Dougherty PM, El-Naggar A, Calin GA, Myers JN. Loss of p53 drives neuron reprogramming in head and neck cancer. Nature 578, 449–454, 2020.Search in Google Scholar

Austin M, Elliott L, Nicolaou N, Grabowska A, Hulse RP. Breast cancer induced nociceptor aberrant growth and collateral sensory axonal branching. Oncotarget 8, 76606–76621, 2017.Search in Google Scholar

Ayala GE, Dai H, Powell M, Li R, Ding Y, Wheeler TM, Shine D, Kadmon D, Thompson T, Miles BJ, Ittmann MM, Rowley D. Cancer-related axonogenesis and neurogenesis in prostate cancer. Clin Cancer Res 14, 7593–7603, 2008.Search in Google Scholar

Bae GE, Kim HS, Won KY, Kim GY, Sung JY, Lim SJ. Lower Sympathetic Nervous System Density and beta-adreno-receptor Expression Are Involved in Gastric Cancer Progression. Anticancer Res 39, 231–236, 2019.Search in Google Scholar

Bakst RL, Wong RJ. Mechanisms of perineural invasion. J Neurol Surg B Skull Base 77, 96–106, 2016.Search in Google Scholar

Bastos DB, Sarafim-Silva BAM, Sundefeld M, Ribeiro AA, Brandao JDP, Biasoli ER, Miyahara GI, Casarini DE, Bernabe DG. Circulating catecholamines are associated with biobehavioral factors and anxiety symptoms in head and neck cancer patients. PLoS One 13, e0202515, 2018.Search in Google Scholar

Blasko F, Krivosikova L, Babal P, Breza J, Trebaticky B, Kuruc R, Mravec B, Janega P. Innervation density and types of nerves in prostate cancer. Neoplasma 70, 101–109, 2023.Search in Google Scholar

Bloom AP, Jimenez-Andrade JM, Taylor RN, Castaneda-Corral G, Kaczmarska MJ, Freeman KT, Coughlin KA, Ghilardi JR, Kuskowski MA, Mantyh PW. Breast cancer-induced bone remodeling, skeletal pain, and sprouting of sensory nerve fibers. J Pain 12, 698–711, 2011.Search in Google Scholar

Campbell LK, Thomas JR, Lamps LW, Smoller BR, Folpe AL. Protein gene product 9.5 (PGP 9.5) is not a specific marker of neural and nerve sheath tumors: an immunohistochemical study of 95 mesenchymal neoplasms. Mod Pathol 16, 963–969, 2003.Search in Google Scholar

Campbell JP, Karolak MR, Ma Y, Perrien DS, Masood-Campbell SK, Penner NL, Munoz SA, Zijlstra A, Yang X, Sterling JA, Elefteriou F. Stimulation of host bone marrow stromal cells by sympathetic nerves promotes breast cancer bone metastasis in mice. PLoS Biol 10, e1001363, 2012.Search in Google Scholar

Coindre JM, de Mascarel A, Trojani M, de Mascarel I, Pages A. Immunohistochemical study of rhabdomyosarcoma. Unexpected staining with S100 protein and cytokeratin. J Pathol 155, 127–132, 1988.Search in Google Scholar

Dadras SS, Lange-Asschenfeldt B, Velasco P, Nguyen L, Vora A, Muzikansky A, Jahnke K, Hauschild A, Hirakawa S,Search in Google Scholar

Mihm MC, Detmar M. Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes. Mod Pathol 18, 1232–1242, 2005.Search in Google Scholar

de Herder WW. Biochemistry of neuroendocrine tumours. Best Pract Res Clin Endocrinol Metab 21, 33–41, 2007.Search in Google Scholar

Djakiew D, Pflug BR, Delsite R, Onoda M, Lynch JH, Arand G, Thompson EW. Chemotaxis and chemokinesis of human prostate tumor cell lines in response to human prostate stromal cell secretory proteins containing a nerve growth factor-like protein. Cancer Res 53, 1416–1420, 1993.Search in Google Scholar

Dolle L, El Yazidi-Belkoura I, Adriaenssens E, Nurcombe V, Hondermarck H. Nerve growth factor overexpression and autocrine loop in breast cancer cells. Oncogene 22, 5592–5601, 2003.Search in Google Scholar

Dwivedi S, Bautista M, Shrestha S, Elhasasna H, Chaphekar T, Vizeacoumar FS, Krishnan A. Sympathetic signaling facilitates progression of neuroendocrine prostate cancer. Cell Death Discov 7, 364, 2021.Search in Google Scholar

Entschladen F, Drell TLt, Lang K, Joseph J, Zaenker KS. Tumour-cell migration, invasion, and metastasis: navigation by neurotransmitters. Lancet Oncol 5, 254–258, 2004.Search in Google Scholar

Entschladen F, Palm D, Lang K, Drell TLt, Zaenker KS. Neoneurogenesis: tumors may initiate their own innervation by the release of neurotrophic factors in analogy to lymphangiogenesis and neoangiogenesis. Med Hypotheses 67, 33–35, 2006.Search in Google Scholar

Entschladen F, Palm D, Drell TLt, Lang K, Zaenker KS. Connecting a tumor to the environment. Curr Pharm Des 13, 3440–3444, 2007.Search in Google Scholar

Entschladen F, Palm D, Niggemann B, Zaenker KS. The cancer‘s nervous tooth: Considering the neuronal crosstalk within tumors. Semin Cancer Biol 18, 171–175, 2008.Search in Google Scholar

Erin N, Akman M, Aliyev E, Tanriover G, Korcum AF. Olvanil activates sensory nerve fibers, increases T cell response and decreases metastasis of breast carcinoma. Life Sci 291, 120305, 2022.Search in Google Scholar

Ermisch B, Schwechheimer K. Protein gene product (PGP) 9.5 in diagnostic (neuro-) oncology. An immunomorpho-logical study. Clin Neuropathol 14, 130–136, 1995.Search in Google Scholar

Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 285, 1182–1186, 1971.Search in Google Scholar

Folkman J, Merler E, Abernathy C, Williams G. Isolation of a tumor factor responsible for angiogenesis. J Exp Med 133, 275–288, 1971.Search in Google Scholar

Geldof AA, Van Haarst EP, Newling DW. Neurotrophic factors in prostate and prostatic cancer. Prostate Cancer Prostatic Dis 1, 236–241, 1998.Search in Google Scholar

Gong J, Korner R, Gaitanos L, Klein R. Exosomes mediate cell contact-independent ephrin-Eph signaling during axon guidance. J Cell Biol 214, 35–44, 2016.Search in Google Scholar

Grabowski P, Schonfelder J, Ahnert-Hilger G, Foss HD, Heine B, Schindler I, Stein H, Berger G, Zeitz M, Scherubl H. Expression of neuroendocrine markers: a signature of human undifferentiated carcinoma of the colon and rectum. Virchows Arch 441, 256–263, 2002.Search in Google Scholar

Grzanna R, Frondoza CG, Hung GL, Sastre A. In vivo administration of propranolol delays development of a murine plasmacytoma tumor. J Auton Nerv Syst 14, 397–401, 1985a.Search in Google Scholar

Grzanna R, Frondoza CG, Otten U. Sympathectomy inhibits growth of a murine plasmacytoma tumor. J Auton Nerv Syst 13, 149–160, 1985b.Search in Google Scholar

Guo K, Ma Q, Li J, Wang Z, Shan T, Li W, Xu Q, Xie K. Interaction of the sympathetic nerve with pancreatic cancer cells promotes perineural invasion through the activation of STAT3 signaling. Mol Cancer Ther 12, 264–273, 2013.Search in Google Scholar

Guo Y, Gil Z. The role of extracellular vesicles in cancer-nerve crosstalk of the peripheral nervous system. Cells 11, 1294, 2022.Search in Google Scholar

Gysler SM, Drapkin R. Tumor innervation: peripheral nerves take control of the tumor microenvironment. J Clin Invest 131, 2021.Search in Google Scholar

Habash FS, Hantash RO, Yunis MA. Assessment of the innervation pattern of oral squamous cell carcinoma using neural protein gene product (9.5)-An immunocytochemical study. J Oral Maxillofac Pathol 16, 16–21, 2012.Search in Google Scholar

Hacker GW, Polak JM, Springall DR, Ballesta J, Cadieux A, Gu J, Trojanowski JQ, Dahl D, Marangos PJ. Antibodies to neurofilament protein and other brain proteins reveal the innervation of peripheral organs. Histochemistry 82, 581–593, 1985.Search in Google Scholar

Hayakawa Y, Sakitani K, Konishi M, Asfaha S, Niikura R, Tomita H, Renz BW, Tailor Y, Macchini M, Middelhoff M, Jiang Z, Tanaka T, Dubeykovskaya ZA, Kim W, Chen X, Urbanska AM, Nagar K, Westphalen CB, Quante M, Lin CS, Gershon MD, Hara A, Zhao CM, Chen D, Worthley DL, Koike K, Wang TC. Nerve growth factor promotes gastric tumorigenesis through aberrant cholinergic signaling. Cancer Cell 31, 21–34, 2017.Search in Google Scholar

Hänze J, Rexin P, Jakubowski P, Schreiber H, Heers H, Lingelbach S, Kinscherf R, Weihe E, Hofmann R, Hegele A. Prostate cancer tissues with positive TMPRSS2-ERG-gene-fusion status may display enhanced nerve density. Urologic Oncology: Seminars and Original Investigations 38, 7–15, 2020.Search in Google Scholar

Hirakawa S, Kodama S, Kunstfeld R, Kajiya K, Brown LF, Detmar M. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 201, 1089–1099, 2005.Search in Google Scholar

Horvathova L, Padova A, Tillinger A, Osacka J, Bizik J, Mravec B. Sympathectomy reduces tumor weight and affects expression of tumor-related genes in melanoma tissue in the mouse. Stress 19, 528–534, 2016.Search in Google Scholar

Hulsurkar M, Li Z, Zhang Y, Li X, Zheng D, Li W. Beta-adrenergic signaling promotes tumor angiogenesis and prostate cancer progression through HDAC2-mediated suppression of thrombospondin-1. Oncogene 36, 1525–1536, 2017.Search in Google Scholar

Chen H, Liu D, Yang Z, Sun L, Deng Q, Yang S, Qian L, Guo L, Yu M, Hu M, Shi M, Guo N. Adrenergic signaling promotes angiogenesis through endothelial cell-tumor cell crosstalk. Endocr Relat Cancer 21, 783–795, 2014.Search in Google Scholar

Kamiya A, Hayama Y, Kato S, Shimomura A, Shimomura T, Irie K, Kaneko R, Yanagawa Y, Kobayashi K, Ochiya T. Genetic manipulation of autonomic nerve fiber innervation and activity and its effect on breast cancer progression. Nat Neurosci 22, 1289–1305, 2019.Search in Google Scholar

Kappos EA, Engels PE, Tremp M, Sieber PK, von Felten S, Madduri S, Meyer Zu Schwabedissen M, Fischmann A, Schaefer DJ, Kalbermatten DF. Denervation leads to volume regression in breast cancer. J Plast Reconstr Aesthet Surg 71, 833–839, 2018.Search in Google Scholar

Keskinov AA, Tapias V, Watkins SC, Ma Y, Shurin MR, Shurin GV. Impact of the sensory neurons on melanoma growth in vivo. PLoS One 11, e0156095, 2016.Search in Google Scholar

Lackovicova L, Banovska L, Bundzikova J, Janega P, Bizik J, Kiss A, Mravec B. Chemical sympathectomy suppresses fibrosarcoma development and improves survival of tumor-bearing rats. Neoplasma 58, 424–429, 2011.Search in Google Scholar

Lang K, Entschladen F, Weidt C, Zaenker KS. Tumor immune escape mechanisms: impact of the neuroendocrine system. Cancer Immunol Immunother 55, 749–760, 2006.Search in Google Scholar

Lopez-Verrilli MA, Picou F, Court FA. Schwann cell-derived exosomes enhance axonal regeneration in the peripheral nervous system. Glia 61, 1795–1806, 2013.Search in Google Scholar

Lu R, Fan C, Shangguan W, Liu Y, Li Y, Shang Y, Yin D, Zhang S, Huang Q, Li X, Meng W, Xu H, Zhou Z, Hu J, Li W, Liu L, Mo X. Neurons generated from carcinoma stem cells support cancer progression. Signal Transduct Target Ther 2, 16036, 2017.Search in Google Scholar

Lucido CT, Wynja E, Madeo M, Williamson CS, Schwartz LE, Imblum BA, Drapkin R, Vermeer PD. Innervation of cervical carcinoma is mediated by cancer-derived exosomes. Gynecol Oncol 154, 228–235, 2019.Search in Google Scholar

Madden KS, Szpunar MJ, Brown EB. β-Adrenergic receptors (β-AR) regulate VEGF and IL-6 production by divergent pathways in high β-AR-expressing breast cancer cell lines. Breast Cancer Res Treat 130, 747–758, 2011.Search in Google Scholar

Madeo M, Colbert PL, Vermeer DW, Lucido CT, Cain JT, Vichaya EG, Grossberg AJ, Muirhead D, Rickel AP, Hong Z, Zhao J, Weimer JM, Spanos WC, Lee JH, Dantzer R, Vermeer PD. Cancer exosomes induce tumor innervation. Nat Commun 9, 4284, 2018.Search in Google Scholar

Magni P, Motta M. Expression of neuropeptide Y receptors in human prostate cancer cells. Ann Oncol 12 Suppl 2, S27–S29, 2001.Search in Google Scholar

Magnon C, Hall SJ, Lin J, Xue X, Gerber L, Freedland SJ, Frenette PS. Autonomic nerve development contributes to prostate cancer progression. Science 341, 1236361, 2013.Search in Google Scholar

Mancino M, Ametller E, Gascon P, Almendro V. The neuronal influence on tumor progression. Biochim Biophys Acta 1816, 105–118, 2011.Search in Google Scholar

Marchesi F, Piemonti L, Mantovani A, Allavena P. Molecular mechanisms of perineural invasion, a forgotten pathway of dissemination and metastasis. Cytokine Growth Factor Rev 21, 77–82, 2010.Search in Google Scholar

Massi D, Puig S, Franchi A, Malvehy J, Vidal-Sicart S, Gonzalez-Cao M, Baroni G, Ketabchi S, Palou J, Santucci M. Tumour lymphangiogenesis is a possible predictor of sentinel lymph node status in cutaneous melanoma: a case-control study. J Clin Pathol 59, 166–173, 2006.Search in Google Scholar

Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics 73, 1907–1920, 2010.Search in Google Scholar

Mauffrey P, Tchitchek N, Barroca V, Bemelmans AP, Firlej V, Allory Y, Romeo PH, Magnon C. Progenitors from the central nervous system drive neurogenesis in cancer. Nature 569, 672–678, 2019.Search in Google Scholar

Meacham CE, Morrison SJ. Tumour heterogeneity and cancer cell plasticity. Nature 501, 328–337, 2013.Search in Google Scholar

Medeiros PJ, Al-Khazraji BK, Novielli NM, Postovit LM, Chambers AF, Jackson DN. Neuropeptide Y stimulates proliferation and migration in the 4T1 breast cancer cell line. Int J Cancer 131, 276–286, 2012.Search in Google Scholar

Mitchell BS, Schumacher U, Kaiserling E. Are tumours innervated? Immunohistological investigations using antibodies against the neuronal marker protein gene product 9.5 (PGP 9.5) in benign, malignant and experimental tumours. Tumour Biol 15, 269–274, 1994a.Search in Google Scholar

Mitchell BS, Schumacher U, Stauber VV, Kaiserling E. Are breast tumours innervated? Immunohistological investigations using antibodies against the neuronal marker protein gene product 9.5 (PGP 9.5) in benign and malignant breast lesions. Eur J Cancer 30A, 1100–1103, 1994b.Search in Google Scholar

Montano X, Djamgoz MB. Epidermal growth factor, neurotrophins and the metastatic cascade in prostate cancer. FEBS Lett 571, 1–8, 2004.Search in Google Scholar

Moretti S, Massi D, Farini V, Baroni G, Parri M, Innocenti S, Cecchi R, Chiarugi P. beta-adrenoceptors are upregulated in human melanoma and their activation releases pro-tumorigenic cytokines and metalloproteases in melanoma cell lines. Lab Invest 93, 279–290, 2013.Search in Google Scholar

Mravec B. Neurobiology of cancer: Definition, historical overview, and clinical implications. Cancer Med 11, 903–921, 2022.Search in Google Scholar

Oertel H. Innervation and tumour growth. The Canadian Medical Association Journal 18, 135–139, 1928.Search in Google Scholar

Olar A, He D, Florentin D, Ding Y, Ayala G. Biologic correlates and significance of axonogenesis in prostate cancer. Hum Pathol 45, 1358–1364, 2014.Search in Google Scholar

Orellana C. Is lymphangiogenesis as important as angiogenesis? Lancet Oncol 6, 265, 2005.Search in Google Scholar

Palm D, Entschladen F. Neoneurogenesis and the neuro-neoplastic synapse. Prog Exp Tumor Res 39, 91–98, 2007.Search in Google Scholar

Palm D, Lang K, Niggemann B, Drell TLt, Masur K, Zaenker KS, Entschladen F. The norepinephrine-driven metastasis development of PC-3 human prostate cancer cells in BALB/c nude mice is inhibited by beta-blockers. Int J Cancer 118, 2744–2749, 2006.Search in Google Scholar

Pereira DB, Sannes T, Dodd SM, Jensen SE, Morgan LS, Chan EK. Life stress, negative mood states, and antibodies to heat shock protein 70 in endometrial cancer. Brain Behav Immun 24, 210–214, 2010.Search in Google Scholar

Polli-Lopes AC, Zucoloto S, de Queiros Cunha F, da Silva Figueiredo LA, Garcia SB. Myenteric denervation reduces the incidence of gastric tumors in rats. Cancer Lett 190, 45–50, 2003.Search in Google Scholar

Prazeres P, Leonel C, Silva WN, Rocha BGS, Santos GSP, Costa AC, Picoli CC, Sena IFG, Goncalves WA, Vieira MS, Costa PAC, Campos L, Lopes MTP, Costa MR, Resende RR, Cunha TM, Mintz A, Birbrair A. Ablation of sensory nerves favours melanoma progression. J Cell Mol Med 24, 9574–9589, 2020.Search in Google Scholar

Pundavela J, Roselli S, Faulkner S, Attia J, Scott RJ, Thorne RF, Forbes JF, Bradshaw RA, Walker MM, Jobling P, Hondermarck H. Nerve fibers infiltrate the tumor microenvironment and are associated with nerve growth factor production and lymph node invasion in breast cancer. Mol Oncol 9, 1626–1635, 2015.Search in Google Scholar

Reavis HD, Chen HI, Drapkin R. Tumor innervation: Cancer has some nerve. Trends Cancer 6, 1059–1067, 2020.Search in Google Scholar

Reeves FA, Battye S, Roth H, Peters JS, Hovens C, Costello AJ, Corcoran NM. Prostatic nerve subtypes independently predict biochemical recurrence in prostate cancer. Journal of Clinical Neuroscience 63, 213–219, 2019.Search in Google Scholar

Renz BW, Takahashi R, Tanaka T, Macchini M, Hayakawa Y, Dantes Z, Maurer HC, Chen X, Jiang Z, Westphalen CB, Ilmer M, Valenti G, Mohanta SK, Habenicht AJR, Middelhoff M, Chu T, Nagar K, Tailor Y, Casadei R, Di Marco M, Kleespies A, Friedman RA, Remotti H, Reichert M, Worthley DL, Neumann J, Werner J, Iuga AC, Olive KP, Wang TC. β2 Adrenergic-neurotrophin feedforward loop promotes pancreatic cancer. Cancer Cell 33, 75–90.e77, 2018a.Search in Google Scholar

Renz BW, Tanaka T, Sunagawa M, Takahashi R, Jiang Z, Macchini M, Dantes Z, Valenti G, White RA, Middelhoff MA, Ilmer M, Oberstein PE, Angele MK, Deng H, Hayakawa Y, Westphalen CB, Werner J, Remotti H, Reichert M, Tailor YH, Nagar K, Friedman RA, Iuga AC, Olive KP, Wang TC. Cholinergic signaling via muscarinic receptors directly and indirectly suppresses pancreatic tumorigenesis and cancer stemness. Cancer Discov 8, 1458–1473, 2018b.Search in Google Scholar

Ricci A, Greco S, Mariotta S, Felici L, Bronzetti E, Cavazzana A, Cardillo G, Amenta F, Bisetti A, Barbolini G. Neurotrophins and neurotrophin receptors in human lung cancer. Am J Respir Cell Mol Biol 25, 439–446, 2001. Search in Google Scholar

Romeo HE, Colombo LL, Esquifino AI, Rosenstein RE, Chuluyan HE, Cardinali DP. Slower growth of tumours in sympathetically denervated murine skin. J Auton Nerv Syst 32, 159–164, 1991.Search in Google Scholar

Saloman JL, Albers KM, Li D, Hartman DJ, Crawford HC, Muha EA, Rhim AD, Davis BM. 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.Search in Google Scholar

Scanlon P, Tian J, Zhong J, Silva I, Shapiro R, Pavlick A, Berman R, Osman I, Darvishian F. Enhanced immunohisto-chemical detection of neural infiltration in primary melanoma: is there a clinical value? Human Pathology 45, 1656–1663, 2014.Search in Google Scholar

Seifert P, Spitznas M. Tumours may be innervated. Virchows Arch 438, 228–231, 2001.Search in Google Scholar

Seifert P, Spitznas M. Axons in human choroidal melanoma suggest the participation of nerves in the control of these tumors. Am J Ophthalmol 133, 711–713, 2002.Search in Google Scholar

Seifert P, Benedic M, Effert P. Nerve fibers in tumors of the human urinary bladder. Virchows Arch 440, 291–297, 2002.Search in Google Scholar

Shan T, Ma J, Ma Q, Guo K, Guo J, Li X, Li W, Liu J, Huang C, Wang F, Wu E. beta2-AR-HIF-1alpha: a novel regulatory axis for stress-induced pancreatic tumor growth and angiogenesis. Curr Mol Med 13, 1023–1034, 2013.Search in Google Scholar

Shao JX, Wang B, Yao YN, Pan ZJ, Shen Q, Zhou JY. Autonomic nervous infiltration positively correlates with pathological risk grading and poor prognosis in patients with lung adenocarcinoma. Thorac Cancer 7, 588–598, 2016.Search in Google Scholar

Shapiro DM, Warren S. Cancer innervation. Cancer Res 9, 707–711, illust, 1949.Search in Google Scholar

Shi M, Liu D, Duan H, Han C, Wei B, Qian L, Chen C, Guo L, Hu M, Yu M, Song L, Shen B, Guo N. Catecholamine up-regulates MMP-7 expression by activating AP-1 and STAT3 in gastric cancer. Mol Cancer 9, 269, 2010.Search in Google Scholar

Shi M, Liu D, Yang Z, Guo N. Central and peripheral nervous systems: master controllers in cancer metastasis. Cancer Metastasis Rev 32, 603–621, 2013.Search in Google Scholar

Schneider MB, Standop J, Ulrich A, Wittel U, Friess H, Andren-Sandberg A, Pour PM. Expression of nerve growth factors in pancreatic neural tissue and pancreatic cancer. J Histochem Cytochem 49, 1205–1210, 2001. Search in Google Scholar

Schoppmann SF. Lymphangiogenesis, inflammation and metastasis. Anticancer Res 25, 4503–4511, 2005. Search in Google Scholar

Silverman HA, Dancho M, Regnier-Golanov A, Nasim M, Ochani M, Olofsson PS, Ahmed M, Miller EJ, Chavan SS, Golanov E, Metz CN, Tracey KJ, Pavlov VA. Brain region-specific alterations in the gene expression of cytokines, immune cell markers and cholinergic system components during peripheral endotoxin-induced inflammation. Mol Med 20, 601–611, 2014.Search in Google Scholar

Silverman DA, Martinez VK, Dougherty PM, Myers JN, Calin GA, Amit M. Cancer-associated neurogenesis and nerve-cancer cross-talk. Cancer Res 81, 1431–1440, 2021.Search in Google Scholar

Sloan EK, Priceman SJ, Cox BF, Yu S, Pimentel MA, Tangkanangnukul V, Arevalo JM, Morizono K, Karanikolas BD, Wu L, Sood AK, Cole SW. The sympathetic nervous system induces a metastatic switch in primary breast cancer. Cancer Res 70, 7042–7052, 2010.Search in Google Scholar

Springall DR, Lackie P, Levene MM, Marangos PJ, Polak JM. Immunostaining of neuron-specific enolase is a valuable aid to the cytological diagnosis of neuroendocrine tumours of the lung. J Pathol 143, 259–265, 1984. Search in Google Scholar

Szpunar MJ, Belcher EK, Dawes RP, Madden KS. Sympathetic innervation, norepinephrine content, and norepinephrine turnover in orthotopic and spontaneous models of breast cancer. Brain Behav Immun 53, 223–233, 2016.Search in Google Scholar

Stavropoulos I, Sarantopoulos A, Liverezas A. Does sympathetic nervous system modulate tumor progression? A narrative review of the literature. J Drug Assess 9, 11, 2020.Search in Google Scholar

Stein-Werblowsky R. The sympathetic nervous system and cancer. Exp Neurol 42, 97–100, 1974.Search in Google Scholar

Strieter RM, Burdick MD, Gomperts BN, Belperio JA, Keane MP. CXC chemokines in angiogenesis. Cytokine Growth Factor Rev 16, 593–609, 2005.Search in Google Scholar

Tatsuta M, Yamamura H, Iishi H, Ichii M, Noguchi S, Baba M, Taniguchi H. Promotion by vagotomy of gastric carcinogenesis induced by N-methyl-N’-nitro-N-nitrosoguanidine in Wistar rats. Cancer Res 45, 194–197, 1985. Search in Google Scholar

Terada T, Matsunaga Y. S-100-positive nerve fibers in hepatocellular carcinoma and intrahepatic cholangiocarcinoma: An immunohistochemical study. Pathology International 51, 89–93, 2001.Search in Google Scholar

Tian T, Zhu YL, Zhou YY, Liang GF, Wang YY, Hu FH, Xiao ZD. Exosome uptake through clathrin-mediated endocytosis and macropinocytosis and mediating miR-21 delivery. J Biol Chem 289, 22258–22267, 2014.Search in Google Scholar

Turner EL, Lane JA, Metcalfe C, Down L, Donovan JL, Hamdy F, Neal D, Vedhara K. Psychological distress and prostate specific antigen levels in men with and without prostate cancer. Brain Behav Immun 23, 1073–1078, 2009.Search in Google Scholar

Vermeer PD. Exosomal induction of tumor innervation. Cancer Res 79, 3529–3535, 2019.Search in Google Scholar

Wacnik PW, Baker CM, Herron MJ, Kren BT, Blazar BR, Wilcox GL, Hordinsky MK, Beitz AJ, Ericson ME. Tumor-induced mechanical hyperalgesia involves CGRP receptors and altered innervation and vascularization of DsRed2 fluorescent hindpaw tumors. Pain 115, 95–106, 2005.Search in Google Scholar

Wang HM, Liao ZX, Komaki R, Welsh JW, O’Reilly MS, Chang JY, Zhuang Y, Levy LB, Lu C, Gomez DR. Improved survival outcomes with the incidental use of beta-blockers among patients with non-small-cell lung cancer treated with definitive radiation therapy. Ann Oncol 24, 1312–1319, 2013.Search in Google Scholar

Xu XT, Xu B, Song QB, Zeng H. The role of neural-related factors in the metastasis of the gastrointestinal cancer. J Cancer Res Ther 9 Suppl, S123–128, 2013.Search in Google Scholar

Xu P, He H, Gu Y, Wang Y, Sun Z, Yang L, Miao C. Surgical trauma contributes to progression of colon cancer by downregulating CXCL4 and recruiting MDSCs. Exp Cell Res 370, 692–698, 2018.Search in Google Scholar

Yaman I, Agac Cobanoglu D, Xie T, Ye Y, Amit M. Advances in understanding cancer-associated neurogenesis and its implications on the neuroimmune axis in cancer. Pharmacol Ther 239, 108199, 2022.Search in Google Scholar

Yang EV, Kim SJ, Donovan EL, Chen M, Gross AC, Webster Marketon JI, Barsky SH, Glaser R. Norepinephrine upregulates VEGF, IL-8, and IL-6 expression in human melanoma tumor cell lines: implications for stress-related enhancement of tumor progression. Brain Behav Immun 23, 267–275, 2009.Search in Google Scholar

Yin L, Hu P, Shi X, Qian W, Zhau HE, Pandol SJ, Lewis MS, Chung LWK, Wang R. Cancer cell’s neuroendocrine feature can be acquired through cell-cell fusion during cancer-neural stem cell interaction. Sci Rep 10, 1216, 2020.Search in Google Scholar

Young HH. On the presence of nerves in tumors and of other structures in them as revealed by a modification of Ehrlich’s method of “Vital Staining” with methylene blue. J Exp Med 11, 1–5, 1897.Search in Google Scholar

Zahalka AH, Arnal-Estape A, Maryanovich M, Nakahara F, Cruz CD, Finley LWS, Frenette PS. Adrenergic nerves activate an angio-metabolic switch in prostate cancer. Science 358, 321–326, 2017.Search in Google Scholar

Zanker KS. The neuro-neoplastic synapse: does it exist? Prog Exp Tumor Res 39, 154–161, 2007.Search in Google Scholar

Zhang D, Park D, Zhong Y, Lu Y, Rycaj K, Gong S, Chen X, Liu X, Chao HP, Whitney P, Calhoun-Davis T, Takata Y, Shen J, Iyer VR, Tang DG. Stem cell and neurogenic gene-expression profiles link prostate basal cells to aggressive prostate cancer. Nat Commun 7, 10798, 2016.Search in Google Scholar

Zhang Z, Lei A, Xu L, Chen L, Chen Y, Zhang X, Gao Y, Yang X, Zhang M, Cao Y. Similarity in gene-regulatory networks suggests that cancer cells share characteristics of embryonic neural cells. J Biol Chem 292, 12842–12859, 2017.Search in Google Scholar

Zhao CM, Hayakawa Y, Kodama Y, Muthupalani S, Westphalen CB, Andersen GT, Flatberg A, Johannessen H, Friedman RA, Renz BW, Sandvik AK, Beisvag V, Tomita H, Hara A, Quante M, Li Z, Gershon MD, Kaneko K, Fox JG, Wang TC, Chen D. Denervation suppresses gastric tumorigenesis. Sci Transl Med 6, 250ra115, 2014.Search in Google Scholar

Zhou H, Shi B, Jia Y, Qiu G, Yang W, Li J, Zhao Z, Lv J, Zhang Y, Li Z. Expression and significance of autonomic nerves and alpha9 nicotinic acetylcholine receptor in colorectal cancer. Mol Med Rep 17, 8423–8431, 2018.Search in Google Scholar

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