Nerve Growth Factor Promotes Gastric Tumorigenesis through Aberrant Cholinergic Signaling

Cancer Cell

Volumn 31, Issue 1, 2017, Pages 21-34

  Hayakawa, Yoku ^a,b   Sakitani, Kosuke ^a   Konishi, Mitsuru ^b   Asfaha, Samuel ^a,c   Niikura, Ryota ^b   Tomita, Hiroyuki ^d   Renz, Bernhard W ^a,e   Tailor, Yagnesh ^a   Macchini, Marina ^a   Middelhoff, Moritz ^a   Jiang, Zhengyu ^a   Tanaka, Takayuki ^a   Dubeykovskaya, Zinaida A ^a   Kim, Woosook ^a   Chen, Xiaowei ^a   Urbanska, Aleksandra M ^a   Nagar, Karan ^a   Westphalen, Christoph B ^a,e   Quante, Michael ^f   Lin, Chyuan Sheng ^a,g   Gershon, Michael D ^a   Hara, Akira ^d   Zhao, Chun Mei ^h   Chen, Duan ^h   Worthley, Daniel L ^a,i   Koike, Kazuhiko ^b   Wang, Timothy C ^a   more..

^a Department of Medicine   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

^d GIFU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^f TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^g II Technische Universität München ^*  (United States)

^h NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

ⁱ UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

acetylcholine; Dclk1; gastric cancer; Lgr5; muscarinic acetylcholine receptor type 3; NGF; stem cell; tuft cell; wnt; YAP

Indexed keywords

ACETYLCHOLINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CHOLINE ACETYLTRANSFERASE; DCLK1 PROTEIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; MUSCARINIC M3 RECEPTOR; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; NEUROTROPHIN 4; PROTEIN; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN; DCAMKL1 PROTEIN, MOUSE; PHOSPHOPROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; YAP PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CHOLINERGIC NERVE; CHOLINERGIC STIMULATION; CHOLINERGIC SYSTEM; COMPARATIVE STUDY; CONTROLLED STUDY; INTESTINE INNERVATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STEM CELL EXPANSION; STOMACH CANCER; STOMACH CARCINOGENESIS; STOMACH EPITHELIUM; STOMACH MUCOSA; ANIMAL; C57BL MOUSE; INNERVATION; PHYSIOLOGY; STOMACH NEOPLASMS;

ACETYLCHOLINE; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; GASTRIC MUCOSA; MICE; MICE, INBRED C57BL; NERVE GROWTH FACTOR; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, MUSCARINIC M3; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS;

EID: 85008318998     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2016.11.005     Document Type: Article

References (66)

1. Aihara, T., Fujishita, T., Kanatani, K., Furutani, K., Nakamura, E., Taketo, M.M., Matsui, M., Chen, D., Okabe, S., Impaired gastric secretion and lack of trophic responses to hypergastrinemia in M3 muscarinic receptor knockout mice. Gastroenterology 125 (2003), 1774–1784.
2. Aihara, T., Nakamura, Y., Taketo, M.M., Matsui, M., Okabe, S., Cholinergically stimulated gastric acid secretion is mediated by M(3) and M(5) but not M(1) muscarinic acetylcholine receptors in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 288 (2005), G1199–G1207.
3. Albo, D., Akay, C.L., Marshall, C.L., Wilks, J.A., Verstovsek, G., Liu, H., Agarwal, N., Berger, D.H., Ayala, G.E., Neurogenesis in colorectal cancer is a marker of aggressive tumor behavior and poor outcomes. Cancer 117 (2011), 4834–4845.
4. Azzolin, L., Panciera, T., Soligo, S., Enzo, E., Bicciato, S., Dupont, S., Bresolin, S., Frasson, C., Basso, G., Guzzardo, V., et al. YAP/TAZ incorporation in the beta-catenin destruction complex orchestrates the Wnt response. Cell 158 (2014), 157–170.
5. Bailey, J.M., Alsina, J., Rasheed, Z.A., McAllister, F.M., Fu, Y.Y., Plentz, R., Zhang, H., Pasricha, P.J., Bardeesy, N., Matsui, W., et al. DCLK1 marks a morphologically distinct subpopulation of cells with stem cell properties in preinvasive pancreatic cancer. Gastroenterology 146 (2014), 245–256.
6. Bannwarth, B., Kostine, M., Targeting nerve growth factor (NGF) for pain management: what does the future hold for NGF antagonists?. Drugs 74 (2014), 619–626.
7. Belkind-Gerson, J., Carreon-Rodriguez, A., Benedict, L.A., Steiger, C., Pieretti, A., Nagy, N., Dietrich, J., Goldstein, A.M., Nestin-expressing cells in the gut give rise to enteric neurons and glial cells. Neurogastroenterol. Motil. 25 (2013), 61–69.e7.
8. Belo, A., Cheng, K., Chahdi, A., Shant, J., Xie, G., Khurana, S., Raufman, J.P., Muscarinic receptor agonists stimulate human colon cancer cell migration and invasion. Am. J. Physiol. Gastrointest. Liver Physiol. 300 (2011), G749–G760.
9. Bezencon, C., Furholz, A., Raymond, F., Mansourian, R., Metairon, S., Le Coutre, J., Damak, S., Murine intestinal cells expressing Trpm5 are mostly brush cells and express markers of neuronal and inflammatory cells. J. Comp. Neurol. 509 (2008), 514–525.
10. Brownell, I., Guevara, E., Bai, C.B., Loomis, C.A., Joyner, A.L., Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell 8 (2011), 552–565.
11. Cai, J., Maitra, A., Anders, R.A., Taketo, M.M., Pan, D., beta-Catenin destruction complex-independent regulation of Hippo-YAP signaling by APC in intestinal tumorigenesis. Genes Dev. 29 (2015), 1493–1506.
12. Ceyhan, G.O., Schafer, K.H., Kerscher, A.G., Rauch, U., Demir, I.E., Kadihasanoglu, M., Bohm, C., Muller, M.W., Buchler, M.W., Giese, N.A., et al. Nerve growth factor and artemin are paracrine mediators of pancreatic neuropathy in pancreatic adenocarcinoma. Ann. Surg. 251 (2010), 923–931.
13. Chandrakesan, P., May, R., Qu, D., Weygant, N., Taylor, V.E., Li, J.D., Ali, N., Sureban, S.M., Qante, M., Wang, T.C., et al. Dclk1+ small intestinal epithelial tuft cells display the hallmarks of quiescence and self-renewal. Oncotarget 6 (2015), 30876–30886.
14. Collins, F., An effect of nerve growth factor on the parasympathetic ciliary ganglion. J. Neurosci. 4 (1984), 1281–1288.
15. Collins, F., Dawson, A., An effect of nerve growth factor on parasympathetic neurite outgrowth. Proc. Natl. Acad. Sci. USA 80 (1983), 2091–2094.
16. da Penha Berzaghi, M., Cooper, J., Castren, E., Zafra, F., Sofroniew, M., Thoenen, H., Lindholm, D., Cholinergic regulation of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) but not neurotrophin-3 (NT-3) mRNA levels in the developing rat hippocampus. J. Neurosci. 13 (1993), 3818–3826.
17. Dolle, L., Adriaenssens, E., El Yazidi-Belkoura, I., Le Bourhis, X., Nurcombe, V., Hondermarck, H., Nerve growth factor receptors and signaling in breast cancer. Curr. Cancer Drug Targets 4 (2004), 463–470.
18. Dubeykovskaya, Z., Si, Y., Chen, X., Worthley, D.L., Renz, B.W., Urbanska, A.M., Hayakawa, Y., Xu, T., Westphalen, C.B., Dubeykovskiy, A., et al. Neural innervation stimulates splenic TFF2 to arrest myeloid cell expansion and cancer. Nat. Commun., 7, 2016, 10517.
19. Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., Bicciato, S., et al. Role of YAP/TAZ in mechanotransduction. Nature 474 (2011), 179–183.
20. Feng, X., Degese, M.S., Iglesias-Bartolome, R., Vaque, J.P., Molinolo, A.A., Rodrigues, M., Zaidi, M.R., Ksander, B.R., Merlino, G., Sodhi, A., et al. Hippo-independent activation of YAP by the GNAQ uveal melanoma oncogene through a trio-regulated rho GTPase signaling circuitry. Cancer Cell 25 (2014), 831–845.
21. Gautam, D., Han, S.J., Hamdan, F.F., Jeon, J., Li, B., Li, J.H., Cui, Y., Mears, D., Lu, H., Deng, C., et al. A critical role for beta cell M3 muscarinic acetylcholine receptors in regulating insulin release and blood glucose homeostasis in vivo. Cell Metab. 3 (2006), 449–461.
22. Gregorieff, A., Liu, Y., Inanlou, M.R., Khomchuk, Y., Wrana, J.L., Yap-dependent reprogramming of Lgr5(+) stem cells drives intestinal regeneration and cancer. Nature 526 (2015), 715–718.
23. Gross, E.R., Gershon, M.D., Margolis, K.G., Gertsberg, Z.V., Li, Z., Cowles, R.A., Neuronal serotonin regulates growth of the intestinal mucosa in mice. Gastroenterology 143 (2012), 408–417.e2.
24. Grundmann, D., Markwart, F., Scheller, A., Kirchhoff, F., Schafer, K.H., Phenotype and distribution pattern of nestin-GFP-expressing cells in murine myenteric plexus. Cell Tissue Res., 2016, 10.1007/s00441-016-2476-9.
25. Hanoun, M., Zhang, D., Mizoguchi, T., Pinho, S., Pierce, H., Kunisaki, Y., Lacombe, J., Armstrong, S.A., Duhrsen, U., Frenette, P.S., Acute myelogenous leukemia-induced sympathetic neuropathy promotes malignancy in an altered hematopoietic stem cell niche. Cell Stem Cell 15 (2014), 365–375.
26. Hayakawa, Y., Ariyama, H., Stancikova, J., Sakitani, K., Asfaha, S., Renz, B.W., Dubeykovskaya, Z.A., Shibata, W., Wang, H., Westphalen, C.B., 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 (2015), 800–814.
27. Hayakawa, Y., Jin, G., Wang, H., Chen, X., Westphalen, C.B., Asfaha, S., Renz, B.W., Ariyama, H., Dubeykovskaya, Z.A., Takemoto, Y., et al. CCK2R identifies and regulates gastric antral stem cell states and carcinogenesis. Gut 64 (2015), 544–553.
28. Hayakawa, Y., Sethi, N., Sepulveda, A.R., Bass, A.J., Wang, T.C., Oesophageal adenocarcinoma and gastric cancer: should we mind the gap?. Nat. Rev. Cancer 16 (2016), 305–318.
29. Hinoi, E., Gao, N., Jung, D.Y., Yadav, V., Yoshizawa, T., Myers, M.G. Jr., Chua, S.C. Jr., Kim, J.K., Kaestner, K.H., Karsenty, G., The sympathetic tone mediates leptin's inhibition of insulin secretion by modulating osteocalcin bioactivity. J. Cell Biol. 183 (2008), 1235–1242.
30. Hirota, C.L., McKay, D.M., M3 muscarinic receptor-deficient mice retain bethanechol-mediated intestinal ion transport and are more sensitive to colitis. Can. J. Physiol. Pharmacol. 84 (2006), 1153–1161.
31. Howard, L., Wyatt, S., Nagappan, G., Davies, A.M., ProNGF promotes neurite growth from a subset of NGF-dependent neurons by a p75NTR-dependent mechanism. Development 140 (2013), 2108–2117.
32. Imajo, M., Ebisuya, M., Nishida, E., Dual role of YAP and TAZ in renewal of the intestinal epithelium. Nat. Cell Biol. 17 (2015), 7–19.
33. Jiao, S., Wang, H., Shi, Z., Dong, A., Zhang, W., Song, X., He, F., Wang, Y., Zhang, Z., Wang, W., et al. A peptide mimicking VGLL4 function acts as a YAP antagonist therapy against gastric cancer. Cancer Cell 25 (2014), 166–180.
34. Kabouridis, P.S., Lasrado, R., McCallum, S., Chng, S.H., Snippert, H.J., Clevers, H., Pettersson, S., Pachnis, V., Microbiota controls the homeostasis of glial cells in the gut lamina propria. Neuron 85 (2015), 289–295.
35. Katayama, Y., Battista, M., Kao, W.M., Hidalgo, A., Peired, A.J., Thomas, S.A., Frenette, P.S., Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124 (2006), 407–421.
36. Kniewallner, K.M., Grimm, N., Humpel, C., Platelet-derived nerve growth factor supports the survival of cholinergic neurons in organotypic rat brain slices. Neurosci. Lett. 574 (2014), 64–69.
37. Kodaira, M., Kajimura, M., Takeuchi, K., Lin, S., Hanai, H., Kaneko, E., Functional muscarinic m3 receptor expressed in gastric cancer cells stimulates tyrosine phosphorylation and MAP kinase. J. Gastroenterol. 34 (1999), 163–171.
38. Lapchak, P.A., Araujo, D.M., Hefti, F., Cholinergic regulation of hippocampal brain-derived neurotrophic factor mRNA expression: evidence from lesion and chronic cholinergic drug treatment studies. Neuroscience 52 (1993), 575–585.
39. Leushacke, M., Ng, A., Galle, J., Loeffler, M., Barker, N., Lgr5+ gastric stem cells divide symmetrically to effect epithelial homeostasis in the pylorus. Cell Rep. 5 (2013), 349–356.
40. Li, X., Nadauld, L., Ootani, A., Corney, D.C., Pai, R.K., Gevaert, O., Cantrell, M.A., Rack, P.G., Neal, J.T., Chan, C.W., et al. Oncogenic transformation of diverse gastrointestinal tissues in primary organoid culture. Nat. Med. 20 (2014), 769–777.
41. Lundgren, O., Jodal, M., Jansson, M., Ryberg, A.T., Svensson, L., Intestinal epithelial stem/progenitor cells are controlled by mucosal afferent nerves. PLoS One, 6, 2011, e16295.
42. Magnon, C., Hall, S.J., Lin, J., Xue, X., Gerber, L., Freedland, S.J., Frenette, P.S., Autonomic nerve development contributes to prostate cancer progression. Science, 341, 2013, 1236361.
43. Mahmoud, A.I., O'Meara, C.C., Gemberling, M., Zhao, L., Bryant, D.M., Zheng, R., Gannon, J.B., Cai, L., Choi, W.Y., Egnaczyk, G.F., et al. Nerves regulate cardiomyocyte proliferation and heart regeneration. Dev. Cell 34 (2015), 387–399.
44. Mendez-Ferrer, S., Michurina, T.V., Ferraro, F., Mazloom, A.R., Macarthur, B.D., Lira, S.A., Scadden, D.T., Ma'ayan, A., Enikolopov, G.N., Frenette, P.S., Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466 (2010), 829–834.
45. Mignone, J.L., Kukekov, V., Chiang, A.S., Steindler, D., Enikolopov, G., Neural stem and progenitor cells in nestin-GFP transgenic mice. J. Comp. Neurol. 469 (2004), 311–324.
46. Neal, K.B., Bornstein, J.C., Mapping 5-HT inputs to enteric neurons of the Guinea-pig small intestine. Neuroscience 145 (2007), 556–567.
47. Okumura, T., Ericksen, R.E., Takaishi, S., Wang, S.S., Dubeykovskiy, Z., Shibata, W., Betz, K.S., Muthupalani, S., Rogers, A.B., Fox, J.G., et al. K-ras mutation targeted to gastric tissue progenitor cells results in chronic inflammation, an altered microenvironment, and progression to intraepithelial neoplasia. Cancer Res. 70 (2010), 8435–8445.
48. Peterson, S.C., Eberl, M., Vagnozzi, A.N., Belkadi, A., Veniaminova, N.A., Verhaegen, M.E., Bichakjian, C.K., Ward, N.L., Dlugosz, A.A., Wong, S.Y., Basal cell carcinoma preferentially arises from stem cells within hair follicle and mechanosensory niches. Cell Stem Cell 16 (2015), 400–412.
49. Quante, M., Bhagat, G., Abrams, J.A., Marache, F., Good, P., Lee, M.D., Lee, Y., Friedman, R., Asfaha, S., Dubeykovskaya, Z., et al. Bile acid and inflammation activate gastric cardia stem cells in a mouse model of Barrett-like metaplasia. Cancer Cell 21 (2012), 36–51.
50. Raufman, J.P., Samimi, R., Shah, N., Khurana, S., Shant, J., Drachenberg, C., Xie, G., Wess, J., Cheng, K., Genetic ablation of M3 muscarinic receptors attenuates murine colon epithelial cell proliferation and neoplasia. Cancer Res. 68 (2008), 3573–3578.
51. Rosenbluh, J., Nijhawan, D., Cox, A.G., Li, X., Neal, J.T., Schafer, E.J., Zack, T.I., Wang, X., Tsherniak, A., Schinzel, A.C., et al. beta-Catenin-driven cancers require a YAP1 transcriptional complex for survival and tumorigenesis. Cell 151 (2012), 1457–1473.
52. Schutz, B., Jurastow, I., Bader, S., Ringer, C., von Engelhardt, J., Chubanov, V., Gudermann, T., Diener, M., Kummer, W., Krasteva-Christ, G., et al. Chemical coding and chemosensory properties of cholinergic brush cells in the mouse gastrointestinal and biliary tract. Front. Physiol., 6, 2015, 87.
53. Shi, G., Zhu, L., Sun, Y., Bettencourt, R., Damsz, B., Hruban, R.H., Konieczny, S.F., Loss of the acinar-restricted transcription factor Mist1 accelerates Kras-induced pancreatic intraepithelial neoplasia. Gastroenterology 136 (2009), 1368–1378.
54. Song, P., Sekhon, H.S., Lu, A., Arredondo, J., Sauer, D., Gravett, C., Mark, G.P., Grando, S.A., Spindel, E.R., M3 muscarinic receptor antagonists inhibit small cell lung carcinoma growth and mitogen-activated protein kinase phosphorylation induced by acetylcholine secretion. Cancer Res. 67 (2007), 3936–3944.
55. Stopczynski, R.E., Normolle, D.P., Hartman, D.J., Ying, H., DeBerry, J.J., Bielefeldt, K., Rhim, A.D., DePinho, R.A., Albers, K.M., Davis, B.M., Neuroplastic changes occur early in the development of pancreatic ductal adenocarcinoma. Cancer Res. 74 (2014), 1718–1727.
56. Tallini, Y.N., Shui, B., Greene, K.S., Deng, K.Y., Doran, R., Fisher, P.J., Zipfel, W., Kotlikoff, M.I., BAC transgenic mice express enhanced green fluorescent protein in central and peripheral cholinergic neurons. Physiol. Genomics 27 (2006), 391–397.
57. Tutton, P.J., Barkla, D.H., Serotonin receptors influencing cell proliferation in the jejunal crypt epithelium and in colonic adenocarcinomas. Anticancer Res. 6 (1986), 1123–1126.
58. Tutton, P.J., Helme, R.D., Proceedings: the role of catecholamines in the regulation of crypt cell proliferation. I. Adrenergic stimulation and blockade. J. Anat. 116 (1973), 467–468.
59. Vaishnavi, A., Le, A.T., Doebele, R.C., TRKing down an old oncogene in a new era of targeted therapy. Cancer Discov. 5 (2015), 25–34.
60. Venkatesh, H.S., Johung, T.B., Caretti, V., Noll, A., Tang, Y., Nagaraja, S., Gibson, E.M., Mount, C.W., Polepalli, J., Mitra, S.S., et al. Neuronal activity promotes glioma growth through Neuroligin-3 secretion. Cell 161 (2015), 803–816.
61. von Moltke, J., Ji, M., Liang, H.E., Locksley, R.M., Tuft-cell-derived IL-25 regulates an intestinal ILC2-epithelial response circuit. Nature 529 (2016), 221–225.
62. Weeraratna, A.T., Dalrymple, S.L., Lamb, J.C., Denmeade, S.R., Miknyoczki, S., Dionne, C.A., Isaacs, J.T., Pan-trk inhibition decreases metastasis and enhances host survival in experimental models as a result of its selective induction of apoptosis of prostate cancer cells. Clin. Cancer Res. 7 (2001), 2237–2245.
63. Westphalen, C.B., Asfaha, S., Hayakawa, Y., Takemoto, Y., Lukin, D.J., Nuber, A.H., Brandtner, A., Setlik, W., Remotti, H., Muley, A., et al. Long-lived intestinal tuft cells serve as colon cancer-initiating cells. J. Clin. Invest. 124 (2014), 1283–1295.
64. Yu, F.X., Zhao, B., Panupinthu, N., Jewell, J.L., Lian, I., Wang, L.H., Zhao, J., Yuan, H., Tumaneng, K., Li, H., et al. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150 (2012), 780–791.
65. Yu, F.X., Luo, J., Mo, J.S., Liu, G., Kim, Y.C., Meng, Z., Zhao, L., Peyman, G., Ouyang, H., Jiang, W., et al. Mutant Gq/11 promote uveal melanoma tumorigenesis by activating YAP. Cancer Cell 25 (2014), 822–830.
66. Zhao, C.M., Hayakawa, Y., Kodama, Y., Muthupalani, S., Westphalen, C.B., Andersen, G.T., Flatberg, A., Johannessen, H., Friedman, R.A., Renz, B.W., et al. Denervation suppresses gastric tumorigenesis. Sci. Transl. Med., 6, 2014, 250ra115.