Login Register Cart 0
Generic placeholder image

Current Cancer Drug Targets

Editor-in-Chief

ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Review Article

Research Progress of Neural Invasion in Pancreatic Cancer

Author(s): Mengying Zhu, Feng Luo, Bin Xu* and Jian Xu*

Volume 24, Issue 4, 2024

Published on: 20 September, 2023

Page: [397 - 410] Pages: 14

DOI: 10.2174/1568009623666230817105221

Price: $65

Abstract

Pancreatic cancer is one of the highly malignant gastrointestinal tumors in humans, and patients suffer from cancer pain in the process of cancer. Most patients suffer from severe pain in the later stages of the disease. The latest studies have shown that the main cause of pain in patients with pancreatic cancer is neuroinflammation caused by tumor cells invading nerves and triggering neuropathic pain on this basis, which is believed to be the result of nerve invasion. Peripheral nerve invasion (PNI), defined as the presence of cancer cells along the nerve or in the epineurial, perineural, and endoneurial spaces of the nerve sheath, is a special way for cancer to spread to distant sites. However, due to limited clinical materials, the research on the mechanism of pancreatic cancer nerve invasion has not been carried out in depth. In addition, perineural invasion is considered to be one of the underlying causes of recurrence and metastasis after pancreatectomy and an independent predictor of prognosis. This article systematically reviewed the neural invasion of pancreatic cancer through bioinformatics analysis, clinical manifestations and literature reviews.

Keywords: Pancreatic cancer, PNI, cancer pain, molecular mechanism, cancer microenvironment, tumor.

« Previous Next »
Graphical Abstract

[1]
Menini, S.; Iacobini, C.; Vitale, M.; Pesce, C.; Pugliese, G. Diabetes and pancreatic cancer-a dangerous liaison relying on carbonyl stress. Cancers (Basel), 2021, 13(2), 313.
[http://dx.doi.org/10.3390/cancers13020313] [PMID: 33467038]
[2]
Kolbeinsson, H.M.; Chandana, S.; Wright, G.P.; Chung, M. Pancreatic cancer: A review of current treatment and novel therapies. J. Invest. Surg., 2023, 36(1), 2129884.
[http://dx.doi.org/10.1080/08941939.2022.2129884] [PMID: 36191926]
[3]
Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J. Clin., 2021, 71(3), 209-249.
[http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]
[4]
Ferlay, J.; Partensky, C.; Bray, F. More deaths from pancreatic cancer than breast cancer in the EU by 2017. Acta Oncol., 2016, 55(9-10), 1158-1160.
[http://dx.doi.org/10.1080/0284186X.2016.1197419] [PMID: 27551890]
[5]
Zhao, C.; Gao, F.; Li, Q.; Liu, Q.; Lin, X. The distributional characteristic and growing trend of pancreatic cancer in China. Pancreas, 2019, 48(3), 309-314.
[http://dx.doi.org/10.1097/MPA.0000000000001222] [PMID: 30855427]
[6]
Hu, J.X.; Zhao, C.F.; Chen, W.B.; Liu, Q.C.; Li, Q.W.; Lin, Y.Y.; Gao, F. Pancreatic cancer: A review of epidemiology, trend, and risk factors. World J. Gastroenterol., 2021, 27(27), 4298-4321.
[http://dx.doi.org/10.3748/wjg.v27.i27.4298] [PMID: 34366606]
[7]
National Cancer Institute. Adult hodgkin lymphoma treatment (PDQ®)–patient version. 2002. Available From: https://www.cancer.gov/types/lymphoma/patient/adult-hodgkin-treatment-pdq
[8]
Tonini, V.; Zanni, M. Pancreatic cancer in 2021: What you need to know to win. World J. Gastroenterol., 2021, 27(35), 5851-5889.
[http://dx.doi.org/10.3748/wjg.v27.i35.5851] [PMID: 34629806]
[9]
Kamisawa, T.; Isawa, T.; Koike, M.; Tsuruta, K.; Okamoto, A. Hematogenous metastases of pancreatic ductal carcinoma. Pancreas, 1995, 11(4), 345-349.
[http://dx.doi.org/10.1097/00006676-199511000-00005] [PMID: 8532650]
[10]
Min, S.K.; You, Y.; Choi, D.W.; Han, I.W.; Shin, S.H.; Yoon, S.; Jung, J.H.; Yoon, S.J.; Heo, J.S. Prognosis of pancreatic head cancer with different patterns of lymph node metastasis. J. Hepatobiliary Pancreat. Sci., 2022, 29(9), 1004-1013.
[http://dx.doi.org/10.1002/jhbp.1159] [PMID: 35446462]
[11]
Avula, L.R.; Hagerty, B.; Alewine, C. Molecular mediators of peritoneal metastasis in pancreatic cancer. Cancer Metastasis Rev., 2020, 39(4), 1223-1243.
[http://dx.doi.org/10.1007/s10555-020-09924-4] [PMID: 32780245]
[12]
Carvajal, G. Pancreatic cancer related pain: Review of pathophysiology and intrathecal drug delivery systems for pain management. Pain Physician, 2021, 24(5), E583-E594.
[PMID: 34323445]
[13]
Liebl, F.; Demir, I.E.; Mayer, K.; Schuster, T.; D’Haese, J.G.; Becker, K.; Langer, R.; Bergmann, F.; Wang, K.; Rosenberg, R.; Novotny, A.R.; Feith, M.; Reim, D.; Friess, H.; Ceyhan, G.O. The impact of neural invasion severity in gastrointestinal malignancies: A clinicopathological study. Ann. Surg., 2014, 260(5), 900-908.
[http://dx.doi.org/10.1097/SLA.0000000000000968] [PMID: 25379860]
[14]
Lindsay, T.H.; Jonas, B.M.; Sevcik, M.A.; Kubota, K.; Halvorson, K.G.; Ghilardi, J.R.; Kuskowski, M.A.; Stelow, E.B.; Mukherjee, P.; Gendler, S.J.; Wong, G.Y.; Mantyh, P.W. Pancreatic cancer pain and its correlation with changes in tumor vasculature, macrophage infiltration, neuronal innervation, body weight and disease progression. Pain, 2005, 119(1-3), 233-246.
[http://dx.doi.org/10.1016/j.pain.2005.10.019] [PMID: 16298491]
[15]
Yao, P.; Ding, Y.Y.; Wang, Z.B.; Ma, J.M.; Hong, T.; Pan, S.N. Effect of gene polymorphism of COMT and OPRM1 on the preoperative pain sensitivity in patients with cancer. Int. J. Clin. Exp. Med., 2015, 8(6), 10036-10039.
[PMID: 26309696]
[16]
Wang, L.; Xu, H.; Ge, Y.; Zhu, H.; Yu, D.; Yu, W.; Lu, Z. Establishment of a murine pancreatic cancer pain model and microarray analysis of pain-associated genes in the spinal cord dorsal horn. Mol. Med. Rep., 2017, 16(4), 4429-4436.
[http://dx.doi.org/10.3892/mmr.2017.7173] [PMID: 28791352]
[17]
Dharaniprasad, G.; Samantaray, A.; Srikanth, L.; Hanumantha Rao, M.; Chandra, A.; Sarma, P.V.G.K. Chronic persistent surgical pain is strongly associated with COMT alleles in patients undergoing cardiac surgery with median sternotomy. Gen. Thorac. Cardiovasc. Surg., 2020, 68(10), 1101-1112.
[http://dx.doi.org/10.1007/s11748-020-01321-6] [PMID: 32100171]
[18]
Meloto, C.B.; Segall, S.K.; Smith, S.; Parisien, M.; Shabalina, S.A.; Rizzatti-Barbosa, C.M.; Gauthier, J.; Tsao, D.; Convertino, M.; Piltonen, M.H.; Slade, G.D.; Fillingim, R.B.; Greenspan, J.D.; Ohrbach, R.; Knott, C.; Maixner, W.; Zaykin, D.; Dokholyan, N.V.; Reenilä, I.; Männistö, P.T.; Diatchenko, L. COMT gene locus. Pain, 2015, 156(10), 2072-2083.
[http://dx.doi.org/10.1097/j.pain.0000000000000273] [PMID: 26207649]
[19]
Lindsay, T.H.; Halvorson, K.G.; Peters, C.M.; Ghilardi, J.R.; Kuskowski, M.A.; Wong, G.Y.; Mantyh, P.W. A quantitative analysis of the sensory and sympathetic innervation of the mouse pancreas. Neuroscience, 2006, 137(4), 1417-1426.
[http://dx.doi.org/10.1016/j.neuroscience.2005.10.055] [PMID: 16388907]
[20]
Chavan, S.S.; Tracey, K.J. Essential neuroscience in immunology. J. Immunol., 2017, 198(9), 3389-3397.
[http://dx.doi.org/10.4049/jimmunol.1601613] [PMID: 28416717]
[21]
Wang, J.; Chen, Y.; Li, X.; Zou, X. Perineural invasion and associated pain transmission in pancreatic cancer. Cancers (Basel), 2021, 13(18), 4594.
[http://dx.doi.org/10.3390/cancers13184594] [PMID: 34572820]
[22]
Yi, S.Q.; Miwa, K.; Ohta, T.; Kayahara, M.; Kitagawa, H.; Tanaka, A.; Shimokawa, T.; Akita, K.; Tanaka, S. Innervation of the pancreas from the perspective of perineural invasion of pancreatic cancer. Pancreas, 2003, 27(3), 225-229.
[http://dx.doi.org/10.1097/00006676-200310000-00005] [PMID: 14508126]
[23]
Schorn, S.; Demir, I.E.; Haller, B.; Scheufele, F.; Reyes, C.M.; Tieftrunk, E.; Sargut, M.; Goess, R.; Friess, H.; Ceyhan, G.O. The influence of neural invasion on survival and tumor recurrence in pancreatic ductal adenocarcinoma – A systematic review and meta-analysis. Surg. Oncol., 2017, 26(1), 105-115.
[http://dx.doi.org/10.1016/j.suronc.2017.01.007] [PMID: 28317579]
[24]
Hishinuma, S.; Ogata, Y.; Tomikawa, M.; Ozawa, I.; Hirabayashi, K.; Igarashi, S. Patterns of recurrence after curative resection of pancreatic cancer, based on autopsy findings. J. Gastrointest. Surg., 2006, 10(4), 511-518.
[http://dx.doi.org/10.1016/j.gassur.2005.09.016] [PMID: 16627216]
[25]
Chen, X.; Liu, F.; Xue, Q.; Weng, X.; Xu, F. Metastatic pancreatic cancer: Mechanisms and detection (Review). Oncol. Rep., 2021, 46(5), 231.
[http://dx.doi.org/10.3892/or.2021.8182] [PMID: 34498718]
[26]
Luo, Y.; Hu, J.; Liu, Y.; Li, L.; Li, Y.; Sun, B.; Kong, R. Invadopodia: A potential target for pancreatic cancer therapy. Crit. Rev. Oncol. Hematol., 2021, 159, 103236.
[http://dx.doi.org/10.1016/j.critrevonc.2021.103236] [PMID: 33482351]
[27]
Blouw, B.; Seals, D.F.; Pass, I.; Diaz, B.; Courtneidge, S.A. A role for the podosome/invadopodia scaffold protein Tks5 in tumor growth in vivo. Eur. J. Cell Biol., 2008, 87(8-9), 555-567.
[http://dx.doi.org/10.1016/j.ejcb.2008.02.008] [PMID: 18417249]
[28]
Xiao, Z.; Luo, G.; Liu, C.; Wu, C.; Liu, L.; Liu, Z.; Ni, Q.; Long, J.; Yu, X. Molecular mechanism underlying lymphatic metastasis in pancreatic cancer. BioMed Res. Int., 2014, 2014, 1-15.
[http://dx.doi.org/10.1155/2014/925845] [PMID: 24587996]
[29]
Li, X.; Wang, Z.; Ma, Q.; Xu, Q.; Liu, H.; Duan, W.; Lei, J.; Ma, J.; Wang, X.; Lv, S.; Han, L.; Li, W.; Guo, J.; Guo, K.; Zhang, D.; Wu, E.; Xie, K. Sonic hedgehog paracrine signaling activates stromal cells to promote perineural invasion in pancreatic cancer. Clin. Cancer Res., 2014, 20(16), 4326-4338.
[http://dx.doi.org/10.1158/1078-0432.CCR-13-3426] [PMID: 24947933]
[30]
Achen, M.G.; Stacker, S.A. Molecular control of lymphatic metastasis. Ann. N. Y. Acad. Sci., 2008, 1131(1), 225-234.
[http://dx.doi.org/10.1196/annals.1413.020] [PMID: 18519975]
[31]
Huh, J.W.; Kim, H.R.; Kim, Y.J. Prognostic value of perineural invasion in patients with stage II colorectal cancer. Ann. Surg. Oncol., 2010, 17(8), 2066-2072.
[http://dx.doi.org/10.1245/s10434-010-0982-7] [PMID: 20182809]
[32]
Chatterjee, D.; Katz, M.H.; Rashid, A.; Wang, H.; Iuga, A.C.; Varadhachary, G.R.; Wolff, R.A.; Lee, J.E.; Pisters, P.W.; Crane, C.H.; Gomez, H.F.; Abbruzzese, J.L.; Fleming, J.B.; Wang, H. Perineural and intraneural invasion in posttherapy pancreaticoduodenectomy specimens predicts poor prognosis in patients with pancreatic ductal adenocarcinoma. Am. J. Surg. Pathol., 2012, 36(3), 409-417.
[http://dx.doi.org/10.1097/PAS.0b013e31824104c5] [PMID: 22301497]
[33]
Jurcak, N.; Zheng, L. Signaling in the microenvironment of pancreatic cancer: Transmitting along the nerve. Pharmacol. Ther., 2019, 200, 126-134.
[http://dx.doi.org/10.1016/j.pharmthera.2019.04.010] [PMID: 31047906]
[34]
Gysler, S.M.; Drapkin, R. Tumor innervation: Peripheral nerves take control of the tumor microenvironment. J. Clin. Invest., 2021, 131(11), e147276.
[http://dx.doi.org/10.1172/JCI147276] [PMID: 34060481]
[35]
Saloman, J.L.; Albers, K.M.; Li, D.; Hartman, D.J.; Crawford, H.C.; Muha, E.A.; Rhim, A.D.; Davis, B.M. Ablation of sensory neurons in a genetic model of pancreatic ductal adenocarcinoma slows initiation and progression of cancer. Proc. Natl. Acad. Sci. USA, 2016, 113(11), 3078-3083.
[http://dx.doi.org/10.1073/pnas.1512603113] [PMID: 26929329]
[36]
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., 2014, 74(6), 1718-1727.
[http://dx.doi.org/10.1158/0008-5472.CAN-13-2050] [PMID: 24448244]
[37]
Bapat, A.A.; Munoz, R.M.; Von Hoff, D.D.; Han, H. Blocking nerve growth factor signaling reduces the neural invasion potential of pancreatic cancer cells. PLoS One, 2016, 11(10), e0165586.
[http://dx.doi.org/10.1371/journal.pone.0165586] [PMID: 27792755]
[38]
Miknyoczki, S.J.; Lang, D.; Huang, L.; Klein-Szanto, A.J.P.; Dionne, C.A.; Ruggeri, B.A. Neurotrophins and Trk receptors in human pancreatic ductal adenocarcinoma: Expression patterns and effects on In vitro invasive behavior. Int. J. Cancer, 1999, 81(3), 417-427.
[http://dx.doi.org/10.1002/(SICI)1097-0215(19990505)81:3<417::AID-IJC16>3.0.CO;2-6] [PMID: 10209957]
[39]
He, S.; Chen, C.H.; Chernichenko, N.; He, S.; Bakst, R.L.; Barajas, F.; Deborde, S.; Allen, P.J.; Vakiani, E.; Yu, Z.; Wong, R.J. GFRα1 released by nerves enhances cancer cell perineural invasion through GDNF-RET signaling. Proc. Natl. Acad. Sci. USA, 2014, 111(19), E2008-E2017.
[http://dx.doi.org/10.1073/pnas.1402944111] [PMID: 24778213]
[40]
Ketterer, K.; Rao, S.; Friess, H.; Weiss, J.; Büchler, M.W.; Korc, M. Reverse transcription-PCR analysis of laser-captured cells points to potential paracrine and autocrine actions of neurotrophins in pancreatic cancer. Clin. Cancer Res., 2003, 9(14), 5127-5136.
[PMID: 14613990]
[41]
Marchesi, F.; Piemonti, L.; Mantovani, A.; Allavena, P. Molecular mechanisms of perineural invasion, a forgotten pathway of dissemination and metastasis. Cytokine Growth Factor Rev., 2010, 21(1), 77-82.
[http://dx.doi.org/10.1016/j.cytogfr.2009.11.001] [PMID: 20060768]
[42]
Marchesi, F.; Piemonti, L.; Fedele, G.; Destro, A.; Roncalli, M.; Albarello, L.; Doglioni, C.; Anselmo, A.; Doni, A.; Bianchi, P.; Laghi, L.; Malesci, A.; Cervo, L.; Malosio, M.; Reni, M.; Zerbi, A.; Di Carlo, V.; Mantovani, A.; Allavena, P. The chemokine receptor CX3CR1 is involved in the neural tropism and malignant behavior of pancreatic ductal adenocarcinoma. Cancer Res., 2008, 68(21), 9060-9069.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-1810] [PMID: 18974152]
[43]
Xu, Q.; Wang, Z.; Chen, X.; Duan, W.; Lei, J.; Zong, L.; Li, X.; Sheng, L.; Ma, J.; Han, L.; Li, W.; Zhang, L.; Guo, K.; Ma, Z.; Wu, Z.; Wu, E.; Ma, Q. Stromal-derived factor-1α/CXCL12-CXCR4 chemotactic pathway promotes perineural invasion in pancreatic cancer. Oncotarget, 2015, 6(7), 4717-4732.
[http://dx.doi.org/10.18632/oncotarget.3069] [PMID: 25605248]
[44]
Koide, N.; Yamada, T.; Shibata, R.; Mori, T.; Fukuma, M.; Yamazaki, K.; Aiura, K.; Shimazu, M.; Hirohashi, S.; Nimura, Y.; Sakamoto, M. Establishment of perineural invasion models and analysis of gene expression revealed an invariant chain (CD74) as a possible molecule involved in perineural invasion in pancreatic cancer. Clin. Cancer Res., 2006, 12(8), 2419-2426.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-1852] [PMID: 16638847]
[45]
Harding, M.A.; Theodorescu, D. RhoGDI signaling provides targets for cancer therapy. Eur. J. Cancer, 2010, 46(7), 1252-1259.
[http://dx.doi.org/10.1016/j.ejca.2010.02.025] [PMID: 20347589]
[46]
Liang, D.; Shi, S.; Xu, J.; Zhang, B.; Qin, Y.; Ji, S.; Xu, W.; Liu, J.; Liu, L.; Liu, C.; Long, J.; Ni, Q.; Yu, X. New insights into perineural invasion of pancreatic cancer: More than pain. Biochim. Biophys. Acta Rev. Cancer, 2016, 1865(2), 111-122.
[http://dx.doi.org/10.1016/j.bbcan.2016.01.002] [PMID: 26794395]
[47]
Witz, I.P.; Levy-Nissenbaum, O. The tumor microenvironment in the post-PAGET era. Cancer Lett., 2006, 242(1), 1-10.
[http://dx.doi.org/10.1016/j.canlet.2005.12.005] [PMID: 16413116]
[48]
Greten, T.F. Myeloid-derived suppressor cells in pancreatic cancer: More than a hidden barrier for antitumour immunity? Gut, 2014, 63(11), 1690-1691.
[http://dx.doi.org/10.1136/gutjnl-2014-306790] [PMID: 24633728]
[49]
Ceyhan, G.O.; Demir, I.E.; Altintas, B.; Rauch, U.; Thiel, G.; Müller, M.W.; Giese, N.A.; Friess, H.; Schäfer, K.H. Neural invasion in pancreatic cancer: A mutual tropism between neurons and cancer cells. Biochem. Biophys. Res. Commun., 2008, 374(3), 442-447.
[http://dx.doi.org/10.1016/j.bbrc.2008.07.035] [PMID: 18640096]
[50]
Bingle, L.; Brown, N.J.; Lewis, C.E. The role of tumour-associated macrophages in tumour progression: Implications for new anticancer therapies. J. Pathol., 2002, 196(3), 254-265.
[http://dx.doi.org/10.1002/path.1027] [PMID: 11857487]
[51]
Zhang, M.; Huang, L.; Ding, G.; Huang, H.; Cao, G.; Sun, X.; Lou, N.; Wei, Q.; Shen, T.; Xu, X.; Cao, L.; Yan, Q. Interferon gamma inhibits CXCL8–CXCR2 axis mediated tumor-associated macrophages tumor trafficking and enhances anti-PD1 efficacy in pancreatic cancer. J. Immunother. Cancer, 2020, 8(1), e000308.
[http://dx.doi.org/10.1136/jitc-2019-000308] [PMID: 32051287]
[52]
Sainz, B., Jr; Martín, B.; Tatari, M.; Heeschen, C.; Guerra, S. ISG15 is a critical microenvironmental factor for pancreatic cancer stem cells. Cancer Res., 2014, 74(24), 7309-7320.
[http://dx.doi.org/10.1158/0008-5472.CAN-14-1354] [PMID: 25368022]
[53]
Jiang, J.; Bai, J.; Qin, T.; Wang, Z.; Han, L. NGF from pancreatic stellate cells induces pancreatic cancer proliferation and invasion by PI3K/AKT/GSK signal pathway. J. Cell. Mol. Med., 2020, 24(10), 5901-5910.
[http://dx.doi.org/10.1111/jcmm.15265] [PMID: 32294802]
[54]
Han, L.; Jiang, J.; Xue, M.; Qin, T.; Xiao, Y.; Wu, E.; Shen, X.; Ma, Q.; Ma, J. Sonic hedgehog signaling pathway promotes pancreatic cancer pain via nerve growth factor. Reg. Anesth. Pain Med., 2020, 45(2), 137-144.
[http://dx.doi.org/10.1136/rapm-2019-100991] [PMID: 31792027]
[55]
Oyama, Y.; Nagao, S.; Na, L.; Yanai, K.; Umebayashi, M.; Nakamura, K.; Nagai, S.; Fujimura, A.; Yamasaki, A.; Nakayama, K.; Morisaki, T.; Onishi, H. TrkB/BDNF signaling could be a new therapeutic target for pancreatic cancer. Anticancer Res., 2021, 41(8), 4047-4052.
[http://dx.doi.org/10.21873/anticanres.15205] [PMID: 34281873]
[56]
Fei, X.; Jin, H.Y.; Gao, Y.; Kong, L.M.; Tan, X.D. Hsa-miR-10a-5p promotes pancreatic cancer growth by BDNF/SEMA4C pathway. J. Biol. Regul. Homeost. Agents, 2020, 34(3), 927-934.
[http://dx.doi.org/10.23812/20-61-A-47] [PMID: 32683841]
[57]
Liu, D.; Song, L.; Dai, Z.; Guan, H.; Kang, H.; Zhang, Y.; Yan, W.; Zhao, X.; Zhang, S. MiR-429 suppresses neurotrophin-3 to alleviate perineural invasion of pancreatic cancer. Biochem. Biophys. Res. Commun., 2018, 505(4), 1077-1083.
[http://dx.doi.org/10.1016/j.bbrc.2018.09.147] [PMID: 30314698]
[58]
Sclabas, G.M.; Fujioka, S.; Schmidt, C.; Li, Z.; Frederick, W.A.I.; Yang, W.; Yokoi, K.; Evans, D.B.; Abbruzzese, J.L.; Hess, K.R.; Zhang, W.; Fidler, I.J.; Chiao, P.J. Overexpression of tropomysin-related kinase B in metastatic human pancreatic cancer cells. Clin. Cancer Res., 2005, 11(2), 440-449.
[http://dx.doi.org/10.1158/1078-0432.440.11.2] [PMID: 15701826]
[59]
Duan, L.; Hu, X.; Feng, D.; Lei, S.; Hu, G. GPC-1 may serve as a predictor of perineural invasion and a prognosticator of survival in pancreatic cancer. Asian J. Surg., 2013, 36(1), 7-12.
[http://dx.doi.org/10.1016/j.asjsur.2012.08.001] [PMID: 23270819]
[60]
Bizzozero, L.; Pergolizzi, M.; Pascal, D.; Maldi, E.; Villari, G.; Erriquez, J.; Volante, M.; Serini, G.; Marchiò, C.; Bussolino, F.; Arese, M. Tumoral neuroligin 1 promotes cancer–nerve interactions and synergizes with the glial cell line-derived neurotrophic factor. Cells, 2022, 11(2), 280.
[http://dx.doi.org/10.3390/cells11020280] [PMID: 35053395]
[61]
Wang, K.; Demir, I.E.; D’Haese, J.G.; Tieftrunk, E.; Kujundzic, K.; Schorn, S.; Xing, B.; Kehl, T.; Friess, H.; Ceyhan, G.O. The neurotrophic factor neurturin contributes toward an aggressive cancer cell phenotype, neuropathic pain and neuronal plasticity in pancreatic cancer. Carcinogenesis, 2014, 35(1), 103-113.
[http://dx.doi.org/10.1093/carcin/bgt312] [PMID: 24067900]
[62]
Li, T.J.; Li, H.; Zhang, W.H.; Xu, S.S.; Jiang, W.; Li, S.; Gao, H.L.; Han, X.; Xu, H.X.; Wu, C.T.; Wang, W.Q.; Yu, X.J.; Liu, L. Human splenic TER cells: A relevant prognostic factor acting via the ARTEMIN-GFRα3-ERK pathway in pancreatic ductal adenocarcinoma. Int. J. Cancer, 2021, 148(7), 1756-1767.
[http://dx.doi.org/10.1002/ijc.33410] [PMID: 33236361]
[63]
Gao, L.; Bo, H.; Wang, Y.; Zhang, J.; Zhu, M. Neurotrophic factor artemin promotes invasiveness and neurotrophic function of pancreatic adenocarcinoma in vivo and in vitro. Pancreas, 2015, 44(1), 134-143.
[http://dx.doi.org/10.1097/MPA.0000000000000223] [PMID: 25243385]
[64]
Hirth, M.; Gandla, J.; Höper, C.; Gaida, M.M.; Agarwal, N.; Simonetti, M.; Demir, A.; Xie, Y.; Weiss, C.; Michalski, C.W.; Hackert, T.; Ebert, M.P.; Kuner, R. CXCL10 and CCL21 promote migration of pancreatic cancer cells toward sensory neurons and neural remodeling in tumors in mice, associated with pain in patients. Gastroenterology, 2020, 159(2), 665-681.e13.
[http://dx.doi.org/10.1053/j.gastro.2020.04.037] [PMID: 32330476]
[65]
Sabbineni, H.; Alwhaibi, A.; Goc, A.; Gao, F.; Pruitt, A.; Somanath, P.R. Genetic deletion and pharmacological inhibition of Akt1 isoform attenuates bladder cancer cell proliferation, motility and invasion. Eur. J. Pharmacol., 2015, 764, 208-214.
[http://dx.doi.org/10.1016/j.ejphar.2015.06.059] [PMID: 26148825]
[66]
Hauser, M.A.; Legler, D.F. Common and biased signaling pathways of the chemokine receptor CCR7 elicited by its ligands CCL19 and CCL21 in leukocytes. J. Leukoc. Biol., 2016, 99(6), 869-882.
[http://dx.doi.org/10.1189/jlb.2MR0815-380R] [PMID: 26729814]
[67]
Koper, O.; Kamińska, J.; Sawicki, K.; Kemona, H. CXCL9, CXCL10, CXCL11, and their receptor (CXCR3) in neuroinflammation and neurodegeneration. Adv. Clin. Exp. Med., 2018, 27(6), 849-856.
[http://dx.doi.org/10.17219/acem/68846] [PMID: 29893515]
[68]
Siegel, R.L.; Miller, K.D.; Fuchs, H.E.; Jemal, A. Cancer statistics, 2021. CA Cancer J. Clin., 2021, 71(1), 7-33.
[http://dx.doi.org/10.3322/caac.21654] [PMID: 33433946]
[69]
Agarwal, B.; Abu-Hamda, E.; Molke, K.L.; Correa, A.M.; Ho, L. Endoscopic ultrasound-guided fine needle aspiration and multidetector spiral CT in the diagnosis of pancreatic cancer. Am. J. Gastroenterol., 2004, 99(5), 844-850.
[http://dx.doi.org/10.1111/j.1572-0241.2004.04177.x] [PMID: 15128348]
[70]
Zhang, L.; Sanagapalli, S.; Stoita, A. Challenges in diagnosis of pancreatic cancer. World J. Gastroenterol., 2018, 24(19), 2047-2060.
[http://dx.doi.org/10.3748/wjg.v24.i19.2047] [PMID: 29785074]
[71]
Zhao, Z.; Liu, W. Pancreatic cancer: A review of risk factors, diagnosis, and treatment. Technol. Cancer Res. Treat., 2020, 19,, 1533033820962117..
[http://dx.doi.org/10.1177/1533033820962117] [PMID: 33357065]
[72]
Rustgi, S.D.; Amin, S.P.; Kim, M.K.; Nagula, S.; Kumta, N.A.; DiMaio, C.J.; Boffetta, P.; Lucas, A.L. Age, socioeconomic features, and clinical factors predict receipt of endoscopic retrograde cholangiopancreatography in pancreatic cancer. World J. Gastrointest. Endosc., 2019, 11(2), 133-144.
[http://dx.doi.org/10.4253/wjge.v11.i2.133] [PMID: 30788032]
[73]
Tang, S.; Huang, G.; Liu, J.; Liu, T.; Treven, L.; Song, S.; Zhang, C.; Pan, L.; Zhang, T. Usefulness of 18F-FDG PET, combined FDG-PET/CT and EUS in diagnosing primary pancreatic carcinoma: A meta-analysis. Eur. J. Radiol., 2011, 78(1), 142-150.
[http://dx.doi.org/10.1016/j.ejrad.2009.09.026] [PMID: 19854016]
[74]
Marrelli, D.; Caruso, S.; Pedrazzani, C.; Neri, A.; Fernandes, E.; Marini, M.; Pinto, E.; Roviello, F. CA19-9 serum levels in obstructive jaundice: Clinical value in benign and malignant conditions. Am. J. Surg., 2009, 198(3), 333-339.
[http://dx.doi.org/10.1016/j.amjsurg.2008.12.031] [PMID: 19375064]
[75]
Kamisawa, T.; Wood, L.D.; Itoi, T.; Takaori, K. Pancreatic cancer. Lancet, 2016, 388(10039), 73-85.
[http://dx.doi.org/10.1016/S0140-6736(16)00141-0] [PMID: 26830752]
[76]
Eibl, G.; Reber, H.A. A xenograft nude mouse model for perineural invasion and recurrence in pancreatic cancer. Pancreas, 2005, 31(3), 258-262.
[http://dx.doi.org/10.1097/01.mpa.0000175176.40045.0f] [PMID: 16163058]
[77]
Bélanger, P.; West, C.R.; Brown, M.T. Development of pain therapies targeting nerve growth factor signal transduction and the strategies used to resolve safety issues. J. Toxicol. Sci., 2018, 43(1), 1-10.
[http://dx.doi.org/10.2131/jts.43.1] [PMID: 29415946]
[78]
Liddle, R.A. The role of transient receptor potential vanilloid 1 (TRPV1) channels in pancreatitis. Biochim. Biophys. Acta Mol. Basis Dis., 2007, 1772(8), 869-878.
[http://dx.doi.org/10.1016/j.bbadis.2007.02.012] [PMID: 17428642]
[79]
Hansford, J.R.; Mulligan, L.M. Multiple endocrine neoplasia type 2 and RET: From neoplasia to neurogenesis. J. Med. Genet., 2000, 37(11), 817-827.
[http://dx.doi.org/10.1136/jmg.37.11.817] [PMID: 11073534]
[80]
Bartscht, T.; Lehnert, H.; Gieseler, F.; Ungefroren, H. The Src family kinase inhibitors PP2 and PP1 effectively block TGF-beta1-induced cell migration and invasion in both established and primary carcinoma cells. Cancer Chemother. Pharmacol., 2012, 70(2), 221-230.
[http://dx.doi.org/10.1007/s00280-012-1904-0] [PMID: 22699812]
[81]
Cederblad, L.; Rosengren, B.; Ryberg, E.; Hermansson, N.O. AZD8797 is an allosteric non-competitive modulator of the human CX3CR1 receptor. Biochem. J., 2016, 473(5), 641-649.
[http://dx.doi.org/10.1042/BJ20150520] [PMID: 26656484]
[82]
Lyu, Z.; Guo, Y.; Gong, Y.; Fan, W.; Dou, B.; Li, N.; Wang, S.; Xu, Y.; Liu, Y.; Chen, B.; Guo, Y.; Xu, Z.; Lin, X. The role of neuroglial crosstalk and synaptic plasticity-mediated central sensitization in acupuncture analgesia. Neural Plast., 2021, 2021, 1-18.
[http://dx.doi.org/10.1155/2021/8881557] [PMID: 33531894]
[83]
Rauch, J N LRP1 is a master regulator of tau uptake and spread. Nature, 2020, 580(7803), 3811-385.
[http://dx.doi.org/10.1038/s41586-020-2156-5]

Rights & Permissions Print Cite
Article Metrics
23
2
© 2024 Bentham Science Publishers | Privacy Policy