Neuroplastic changes occur early in the development of pancreatic ductal adenocarcinoma

Cancer Research

Volumn 74, Issue 6, 2014, Pages 1718-1727

  Stopczynski, Rachelle E ^a   Normolle, Daniel P ^b   Hartman, Douglas J ^c   Ying, Haoqiang ^d   DeBerry, Jennifer J ^a   Bielefeldt, Klaus ^a   Rhim, Andrew D ^f   DePinho, Ronald A ^e   Albers, Kathryn M ^a   Davis, Brian M ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b Departments Biostatistics   (United States)

^c Departments of Pathology   (United States)

^d Departments of Genomic Medicine   (United States)

^e UNIVERSITY OF TEXAS   (United States)

^f UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; GROWTH FACTOR RECEPTOR; NEUROTROPHIC FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CARCINOGENESIS; CELIAC GANGLION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; EXPLORATORY BEHAVIOR; FEMALE; GENE EXPRESSION; GENE MUTATION; MALE; METASTASIS; MOUSE; NERVE CELL PLASTICITY; NEUROGENIC INFLAMMATION; NONHUMAN; PAIN THRESHOLD; PANCREAS ADENOCARCINOMA; PANCREAS ADENOMA; PANCREATIC NERVE; PANCREATITIS; PERINEURAL INVASION; PERIPHERAL NERVE; PERIPHERAL NERVOUS SYSTEM FUNCTION; PRIORITY JOURNAL; SENSORY GANGLION; SENSORY NERVE; SPINAL CORD METASTASIS;

ANIMALS; AUTONOMIC FIBERS, POSTGANGLIONIC; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; GANGLIA, SYMPATHETIC; HUMANS; HYPERTROPHY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE GROWTH FACTORS; NEURONS, AFFERENT; PANCREAS; PANCREATIC NEOPLASMS; RECEPTORS, NERVE GROWTH FACTOR; SPINAL CORD NEOPLASMS; TRANSCRIPTOME;

EID: 84896496826     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-2050     Document Type: Article

References (50)

1. Ceyhan GO, Bergmann F, Kadihasanoglu M, Altintas B, Demir IE, Hinz U, et al. Pancreatic neuropathy and neuropathic pain-A comprehensive pathomorphological study of 546 cases. Gastroenterology 2009;136:177-86.e1.
2. Ceyhan GO, Scḧafer K-H, Kerscher AG, Rauch U, Demir IE, Kadihasanoglu M, et al. Nerve growth factor and artemin are paracrine mediators of pancreatic neuropathy in pancreatic adenocarcinoma. Ann Surg 2010;251:923-31.
3. Ceyhan GO, Giese NA, Erkan M, Kerscher AG, Wente MN, Giese T, et al. The neurotrophic factor artemin promotes pancreatic cancer invasion. Ann Surg 2006;244:274-81. (Pubitemid 44305543)
4. Ma J, Jiang Y, Jiang Y, Sun Y, Zhao X. Expression of nerve growth factor and tyrosine kinase receptor A and correlation with perineural invasion in pancreatic cancer. J Gastroenterol Hepatol 2008;23: 1852-9.
5. Zeng Q, Cheng Y, Zhu Q, Yu Z, Wu X, Huang K, et al. The relationship between over-expression of glial cell-derived neurotrophic factor and its RET receptor with progression and prognosis of human pancreatic cancer. J Int Med Res 2008;36:656-64.
6. Zhu BZ, Friess H, diMola FF, Zimmermann A, Graber HU, Korc M, et al. Nerve growth factor expression correlates with perineural invasion and pain in human pancreatic cancer. J Clin Oncol 1999;17:2419-28. (Pubitemid 29368241)
7. Magnon C, Hall SJ, Lin J, Xue X, Gerber L, Freedland SJ, et al. Autonomic nerve development contributes to prostate cancer progression. Science 2013;341:1236361.
8. Schwartz ES, Christianson JA, Chen X, La J-H, Davis BM, Albers KM, et al. Synergistic role of TRPV1 and TRPA1 in pancreatic pain and inflammation. Gastroenterology 2010;1283-91.
9. Schwartz ES, La J-H, Scheff NN, Davis BM, Albers KM, Gebhart GF. TRPV1 and TRPA1 antagonists prevent the transition of acute to chronic inflammation and pain in chronic pancreatitis. J Neurosci 2013;33:5603-11.
10. Tuveson DA, Shaw AT, Willis NA, Silver DP, Jackson EL, Chang S, et al. Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 2004;5:375-87. (Pubitemid 38482073)
11. Bardeesy N, Aguirre AJ, Chu GC, Cheng K-H, Lopez LV, Hezel AF, et al. Both p16(Ink4a) and the p19(Arf)-p53 pathway constrain progression of pancreatic adenocarcinoma in the mouse. Proc Natl Acad Sci U S A 2006;103:5947-52.
12. Hruban RH, Adsay NV, Albores-Saavedra J, Anver MR, Biankin AV, Boivin GP, et al. Pathology of genetically engineered mouse models of pancreatic exocrine cancer: consensus report and recommendations. Cancer Res 2006;66:95-106. (Pubitemid 43166014)
13. Rhim AD, Mirek ET, Aiello NM, Maitra A, Bailey JM, McAllister F, et al. EMT and dissemination precede pancreatic tumor formation. Cell; 2012;148:349-61.
14. Sevcik MA, Jonas BM, Lindsay TH, Halvorson KG, Ghilardi JR, Kuskowski MA, et al. Endogenous opioids inhibit early-stage pancreatic pain in a mouse model of pancreatic cancer. Gastroenterology 2006;131:900-10. (Pubitemid 44316822)
15. Meijering E, Jacob M, Sarria J-CF, Steiner P, Hirling H, Unser M. Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 2004;58:167-76. (Pubitemid 38509178)
16. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-Time quantitative PCR and the 2(DDC(T)) method. Methods 2001;25:402-8. (Pubitemid 34164012)
17. Takahashi T, Ishikura H, Motohara T. Perineural invasion by ductal adenocarcinoma of the pancreas. J Surg Oncol 1997;65:164-70. (Pubitemid 27351703)
18. Liebig C, Ayala G, Wilks JA, Berger DH, Albo D. Perineural invasion in cancer: a review of the literature. Cancer 2009;115:3379-91.
19. Bapat AA, Hostetter G, Von Hoff DD, Han H. Perineural invasion and associated pain in pancreatic cancer. Nat Rev Cancer 2011;11: 695-707.
20. Liu B, Lu K-Y. Neural invasion in pancreatic carcinoma. Hepatobiliary Pancreat Dis Int 2002;1:469-76. (Pubitemid 36748789)
21. Mitsunaga S, Hasebe T, Kinoshita T, Konishi M, Takahashi S, Gotohda N, et al. Detail histologic analysis of nerve plexus invasion in invasive ductal carcinoma of the pancreas and its prognostic impact.AmJ Surg Pathol 2007;31:1636-44.
22. Nakao A, Harada A, Nonami T, Kaneko T, Takagi H. Clinical significance of carcinoma invasion of the extrapancreatic nerve plexus in pancreatic cancer. Pancreas 1996;12:357-61. (Pubitemid 26138628)
23. Fasanella KE, Christianson JA, Chanthaphavong RS, Davis BM. Distribution and neurochemical identification of pancreatic afferents in the mouse. J Comp Neurol 2008;509:42-52. (Pubitemid 351846399)
24. Romac JMJ, McCall SJ, Humphrey JE, Heo J, Liddle RA. Pharmacologic disruption of TRPV1-expressing primary sensory neurons but not genetic deletion of TRPV1 protects mice against pancreatitis. Pancreas 2008;36:394-401. (Pubitemid 351591582)
25. Liddle RA, Nathan JD. Neurogenic inflammation and pancreatitis. Pancreatology 2004;4:551-9; discussion 559-60. (Pubitemid 40091406)
26. Zhu Y, Colak T, Shenoy M, Liu L, Pai R, Li C, et al. Nerve growth factor modulates TRPV1 expression and function and mediates pain in chronic pancreatitis. Gastroenterology 2011;141:370-7.
27. Nathan JD, Peng RY, Wang Y, McVey DC, Vigna SR, Liddle RA. Primary sensory neurons: a common final pathway for inflammation in experimental pancreatitis in rats. Am J Physiol Gastrointest Liver Physiol 2002;283:G938-46. (Pubitemid 35033937)
28. Ceyhan GO, Michalski CW, Demir IE, M̈uller MW, Friess H. Pancreatic pain. Best Pract Res Clin Gastroenterol 2008;22:31-44.
29. Lindsay TH, Jonas BM, Sevcik MA, Kubota K, Halvorson KG, Ghilardi JR, et al. Pancreatic cancer pain and its correlation with changes in tumor vasculature, macrophage infiltration, neuronal innervation, body weight and disease progression. Pain 2005;119:233-46. (Pubitemid 41752984)
30. Dang C, Zhang Y, Ma Q, Shimahara Y. Expression of nerve growth factor receptors is correlated with progression and prognosis of human pancreatic cancer. J Gastroenterol Hepatol 2006;21:850-8. (Pubitemid 43793283)
31. Ceyhan GO, Demir IE, Altintas B, Rauch U, Thiel G, M̈uller MW, et al. Neural invasion in pancreatic cancer: a mutual tropism between neurons and cancer cells. Biochem Biophys Res Commun 2008;374: 442-7.
32. Airaksinen MS, Saarma M. The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci 2002;3:383-94. (Pubitemid 135706635)
33. Huang EJ, Reichardt LF. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 2001;24:677-736. (Pubitemid 32695243)
34. Molliver DC, Lindsay J, Albers KM, Davis BM. Overexpression of NGF or GDNF alters transcriptional plasticity evoked by inflammation. Pain 2005;113:277-84. (Pubitemid 40127508)
35. Wang S, Elitt CM, Malin SA, Albers KM. Effects of the neurotrophic factor artemin on sensory afferent development and sensitivity. Sheng Li Xue Bao 2008;60:565-70.
36. Elitt CM, McIlwrath SL, Lawson JJ, Malin SA, Molliver DC, Cornuet PK, et al. Artemin overexpression in skin enhances expression of TRPV1 and TRPA1 in cutaneous sensory neurons and leads to behavioral sensitivity to heat and cold. J Neurosci 2006;26:8578-87. (Pubitemid 44316187)
37. Malin SA, Davis BM. Postnatal roles of glial cell line-derived neurotrophic factor family members in nociceptors plasticity. Sheng Li Xue Bao 2008;60:571-8.
38. Shu X, Mendell LM. Nerve growth factor acutely sensitizes the response of adult rat sensory neurons to capsaicin. Neurosci Lett 1999;274:159-62. (Pubitemid 29462536)
39. Ciobanu C, Reid G, Babes A. Acute and chronic effects of neurotrophic factors BDNF and GDNF on responses mediated by thermo-sensitive TRP channels in cultured rat dorsal root ganglion neurons. Brain Res 2009;1284:54-67.
40. Schmutzler BS, Roy S, Hingtgen CM. Glial cell line-derived neurotrophic factor family ligands enhance capsaicin-stimulated release of calcitonin gene-related peptide from sensory neurons. Neuroscience 2009;161:148-56.
41. Gil Z, Cavel O, Kelly K, Brader P, Rein A, Gao SP, et al. Paracrine regulation of pancreatic cancer cell invasion by peripheral nerves. J Natl Cancer Inst 2010;102:107-18.
42. Ceyhan GO, Bergmann F, Kadihasanoglu M, Erkan M, Park W, Hinz U, et al. The neurotrophic factor artemin influences the extent of neural damage and growth in chronic pancreatitis. Gut 2007;56: 534-44. (Pubitemid 46580510)
43. Guerra C, Collado M, Navas C, Schuhmacher AJ, Hernandez-Porras I, Canamero M, et al. Pancreatitis-induced inflammation contributes to pancreatic cancer by inhibiting oncogene-induced senescence. Cancer Cell 2011;19:728-39.
44. Whitcomb DC, Pogue-Geile K. Pancreatitis as a risk for pancreatic cancer. Gastroenterol Clin North Am 2002;31:663-78. (Pubitemid 34761231)
45. Carriere C, Young AL, Gunn JR, Longnecker DS, Korc M. Acute pancreatitis markedly accelerates pancreatic cancer progression in mice expressing oncogenic Kras. Biochem Biophys Res Commun 2009;382:561-5.
46. Guerra C, Schuhmacher AJ, Canamero M, Grippo PJ, Verdaguer L, Perez-Gallego L, et al. Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell 2007;11:291-302. (Pubitemid 46349841)
47. Carriere C, Young AL, Gunn JR, Longnecker DS, Korc M. Acute pancreatitis accelerates initiation and progression to pancreatic cancer in mice expressing oncogenic Kras in the nestin cell lineage. PLoS ONE 2011;6:e27725.
48. Fukuda A, Wang SC, Morris JP, Folias AE, Liou A, Kim GE, et al. Stat3 and MMP7 contribute to pancreatic ductal adenocarcinoma initiation and progression. Cancer Cell 2011;19:441-55.
49. Lillemoe KD, Cameron JL, Kaufman HS, Yeo CJ, Pitt HA, Sauter PK. Chemical splanchnicectomy in patients with unresectable pancreatic cancer: a prospective randomized trial. Ann Surg 1993;217:447-55; discussion 456-7.
50. Wong GY, Schroeder DR, Carns PE, Wilson JL, Martin DP, Kinney MO, et al. Effect of neurolytic celiac plexus block on pain relief, quality of life, and survival in patients with unresectable pancreatic cancer a randomized control trial. JAMA 2004;291:1092-9. (Pubitemid 38541686)