Advances in Mechanisms of Neurotropism Correlated to Perineural Invasion in Pancreatic Cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

ZHANG Yong , YAN Yu ,  DANG Chengxue.

Department of Oncological Surgery, The First Affliated Hospital of Medical College, Xi’an Jiaotong University, Xi’an 710061, Shaanxi Province, China;

Corresponding author：

DANG Chengxue., Email: dangchengxue@yahoo.com.cn

Keywords：

Pancreatic cancer; Perineural invasion; Neurotropism; Nerve growth factor; Tumor-nerve microenvironment

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ObjectiveTo explore the mechanisms of perineural invasion (PNI) in pancreatic cancer so as to find a new treatment for pancreatic cancer. MethodsThe literatures on PNI, neurotropism, nerve-tumor microenvironment and nerve growth factor in pancreatic cancer were reviewed and the mechanisms of PNI were summarized. ResultsThe rich innervation of pancreatic tissue itself and the minute slits within perineural structure were the anatomic basis of PNI. Tumor cells expressed neural antigens were the pathological basis of PNI. Tumor-nerve microenvironment and nerve growth factor family and themselves receptors might play an important molecular role in PNI. However, tumor cells expressed neural antigens were not only closely related to the PNI, but also the interaction between tumor cells and nerves played an important role in PNI. ConclusionsThe detailed mechanisms of PNI are extremely complex and controversial up to today. However, it is possible to search a new therapeutic target in pancreatic cancer according to the mechanisms of PNI.

Citation： ZHANG Yong,YAN Yu,DANG Chengxue.. Advances in Mechanisms of Neurotropism Correlated to Perineural Invasion in Pancreatic Cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2011, 18(1): 21-25. doi: Copy

1.	Kleeff J, Michalski C, Friess H, et al. Pancreatic cancer: from bench to 5year survival [J]. Pancreas, 2006, 33(2): 111118.
2.	Van den Broeck A, Sergeant G, Ectors N, et al. Patterns of recurrence after curative resection of pancreatic ductal adenocarcinoma [J]. Eur J Surg Oncol, 2009, 35(6): 600604.
3.	Keleg S, Büchler P, Ludwig R, et al. Invasion and metastasis in pancreatic cancer [J]. Mol Cancer, 2003, 2: 14.
4.	Akert K, Sandri C, Weibel ER, et al. The fine structure of the perineural endothelium [J]. Cell Tissue Res, 1976, 165(3): 281295.
5.	Batsakis JG. Nerves and neurotropic carcinomas [J]. Ann Otol Rhinol Laryngol, 1985, 94(4 Pt 1): 426427.
6.	Okamoto M, Nakamura Y, Imaizumi M. Peripheral nerve structure [J]. Saishin Igaku, 1968, 23(11): 22402252.
7.	党诚学, 王健生, 任予, 等. 胰腺癌神经浸润途径的探讨和临床意义的研究 [J]. 中华肝胆外科杂志, 2001, 7(6): 357358.
8.	Rodin AE, Larson DL, Roberts DK. Nature of the perineural space invaded by prostatic carcinoma [J]. Cancer, 1967, 20(10): 17721779.
9.	Ballantyne AJ, Mccarten AB, Ibanez ML. The extension of cancer of the head and neck through peripheral nerves [J]. Am J Surg， 1963, 106: 651667.
10.	Kayahara M, Nakagawara H, Kitagawa H, et al. The nature of neural invasion by pancreatic cancer [J]. Pancreas, 2007, 35(3): 218223.
11.	Beger HG, Rau B, Gansauge F, et al. Treatment of pancreatic cancer: challenge of the facts [J]. World J Surg, 2003, 27(10): 10751084.
12.	Dang C, Zhang Y, Ma Q, et al. Expression of nerve growth factor receptors is correlated with progression and prognosis of human pancreatic cancer [J]. J Gastroenterol Hepatol, 2006, 21(5): 850858.
13.	Zhu Z, Friess H, diMola FF, et al. Nerve growth factor expression correlates with perineural invasion and pain in human pancreatic cancer [J]. J Clin Oncol, 1999, 17(8): 24192428.
14.	di Mola FF, di Sebastiano P. Pain and pain generation in pancreatic cancer [J]. Langenbecks Arch Surg, 2008, 393(6): 919922.
15.	Pour PM, Bell RH, Batra SK. Neural invasion in the staging of pancreatic cancer [J]. Pancreas, 2003, 26(4): 322325.
16.	Ozaki H, Hiraoka T, Mizumoto R, et al. The prognostic significance of lymph node metastasis and intrapancreatic perineural invasion in pancreatic cancer after curative resection [J]. Surg Today, 1999, 29(1): 1622.
17.	Cruveilhier J, Maladies des nerfs. Anatomic Pathologique du Corps Humain [M]. 2nd ed. Paris: J.B. Baillière, 1835: 3335.
18.	Ernst P. Uber das Wachstum und die Verbeitung bosartiger Geshwulstte, insbesondere des Krebes in den Lymphbahnen der Nerven [J]. Beitr Path Anat, 1905, 7(Suppl): 2951.
19.	Kuwayti K, Baggenstoss AH, Stauffer MH, et al. Carcinoma of the major intrahepatic and the extrahepatic bile ducts exclusive of the papilla of Vater [J]. Surg Gynecol Obstet, 1957, 104(3): 357366.
20.	Dunn M, Morgan MB, Beer TW. Perineural invasion: identification, significance, and a standardized definition [J]. Dermatol Surg, 2009, 35(2): 214221.
21.	Liebig C, Ayala G, Wilks JA, et al. Perineural invasion in cancer: a review of the literature [J]. Cancer, 2009, 115(15): 33793391.
22.	Znker KS, Entschladen F (eds): Neuronal activity in tumor tissue [A]. In: Progression in Experimental Tumor Research [M]. Basel: Karger, 2007: 132133.
23.	Eibl G, Reber HA. A xenograft nude mouse model for perineural invasion and recurrence in pancreatic cancer [J]. Pancreas, 2005, 31(3): 258262.
24.	Carlson JA, Dickersin GR, Sober AJ, et al. Desmoplastic neurotropic melanoma. A clinicopathologic analysis of 28 cases [J]. Cancer, 1995, 75(2): 478494.
25.	Watanabe H, Mizutani T, Haraguchi T, et al. SWI/SNF complex is essential for NRSFmediated suppression of neuronal genes in human nonsmall cell lung carcinoma cell lines [J]. Oncogene, 2006, 25(3): 470479.
26.	Chédotal A, Kerjan G, MoreauFauvarque C. The brain within the tumor: new roles for axon guidance molecules in cancers [J]. Cell Death Differ, 2005, 12(8): 10441056.
27.	Zhu Z, Kleeff J, Kayed H, et al. Nerve growth factor and enhancement of proliferation, invasion, and tumorigenicity of pancreatic carcinomas cells [J]. Mol Carcinog, 2002, 35(3): 138147.
28.	Zhang Y, Dang C, Ma Q, et al. Expression of nerve growth factor receptors and their prognostic value in human pancreatic cancer [J]. Oncol Rep, 2005, 14(1): 161171.
29.	Bockman DE, Büchler M, Beger HG. Interaction of pancreatic ductal carcinoma with nerves leads to nerve damage [J]. Gastroenterology, 1994, 107(1): 219230.
30.	郑善川, 梁丽, 张玉茹, 等. GDNF及其受体Ret在腺样囊性癌嗜神经侵袭和细胞增殖中作用的初步研究 [J]. 口腔医学研究, 2010, 26(3): 380383.
31.	Ceyhan GO, Giese NA, Erkan M, et al. The neurotrophic factor artemin promotes pancreatic cancer invasion [J]. Ann Surg, 2006, 244(2): 274281.
32.	朱栋良, 罗地来, 罗刚, 等. Artemin、GFRα3在胰腺癌中的表达及其与胰腺癌神经浸润转移的相关性 [J]. 南方医科大学学报, 2009, 29(3): 428431.
33.	Ben QW, Wang JC, Liu J, et al. Positive expression of L1CAM is associated with perineural invasion and poor outcome in pancreatic ductal adenocarcinoma [J]. Ann Surg Oncol, 2010, 17(8): 22132221.
34.	Farrow B, Albo D, Berger DH. The role of the tumor microenvironment in the progression of pancreatic cancer [J]. J Surg Res, 2008, 149(2): 319328.
35.	Ma J, Jiang Y, Jiang Y, et al. Expression of nerve growth factor and tyrosine kinase receptor A and correlation with perineural invasion in pancreatic cancer [J]. J Gastroenterol Hepatol, 2008, 23(12): 18521859.
36.	Okada Y, Eibl G, Duffy JP, et al. Glial cellderived neurotrophic factor upregulates the expression and activation of matrix metalloproteinase9 in human pancreatic cancer [J]. Surgery, 2003, 134(2): 293299.
37.	Iwahashi N, Nagasaka T, Tezel G, et al. Expression of glial cell linederived neurotrophic factor correlates with perineural invasion of bile duct carcinoma [J]. Cancer, 2002, 94(1): 167174.
38.	Podratz JL, Rodriguez E, Windebank AJ. Role of the extracellular matrix in myelination of peripheral nerve [J]. Glia, 2001, 35(1): 3540.
39.	Hill RE, Williams RE. A quantitative analysis of perineurial cell basement membrane collagen Ⅳ, laminin and fibronectin in diabetic and nondiabetic human sural nerve [J]. J Anat, 2002, 201(2): 185192.
40.	Vega JA, Esteban I, Naves FJ, et al. Immunohistochemical localization of laminin and type Ⅳ collagen in human cutaneous sensory nerve formations [J]. Anat Embryol (Berl), 1995, 191(1): 3339.
41.	Ryschich E, Khamidjanov A, Kerkadze V, et al. Promotion of tumor cell migration by extracellular matrix proteins in human pancreatic cancer [J]. Pancreas, 2009, 38(7): 804810.
42.	Wang W, Zhao H, Zhang S, et al. Patterns of expression and function of the p75NGFR protein in pancreatic cancer cells and tumours [J]. Eur J Surg Oncol, 2009, 35(8): 826832.
43.	Yao J, Ma Q, Wang L, et al. Pleiotrophin expression in human pancreatic cancer and its correlation with clinicopathological features, perineural invasion, and prognosis [J]. Dig Dis Sci, 2009, 54(4): 895901.
44.	Abiatari I, DeOliveira T, Kerkadze V, et al. Consensus transcriptome signature of perineural invasion in pancreatic carcinoma [J]. Mol Cancer Ther, 2009, 8(6): 14941504.

1. Kleeff J, Michalski C, Friess H, et al. Pancreatic cancer: from bench to 5year survival [J]. Pancreas, 2006, 33(2): 111118.
2. Van den Broeck A, Sergeant G, Ectors N, et al. Patterns of recurrence after curative resection of pancreatic ductal adenocarcinoma [J]. Eur J Surg Oncol, 2009, 35(6): 600604.
3. Keleg S, Büchler P, Ludwig R, et al. Invasion and metastasis in pancreatic cancer [J]. Mol Cancer, 2003, 2: 14.
4. Akert K, Sandri C, Weibel ER, et al. The fine structure of the perineural endothelium [J]. Cell Tissue Res, 1976, 165(3): 281295.
5. Batsakis JG. Nerves and neurotropic carcinomas [J]. Ann Otol Rhinol Laryngol, 1985, 94(4 Pt 1): 426427.
6. Okamoto M, Nakamura Y, Imaizumi M. Peripheral nerve structure [J]. Saishin Igaku, 1968, 23(11): 22402252.
7. 党诚学, 王健生, 任予, 等. 胰腺癌神经浸润途径的探讨和临床意义的研究 [J]. 中华肝胆外科杂志, 2001, 7(6): 357358.
8. Rodin AE, Larson DL, Roberts DK. Nature of the perineural space invaded by prostatic carcinoma [J]. Cancer, 1967, 20(10): 17721779.
9. Ballantyne AJ, Mccarten AB, Ibanez ML. The extension of cancer of the head and neck through peripheral nerves [J]. Am J Surg， 1963, 106: 651667.
10. Kayahara M, Nakagawara H, Kitagawa H, et al. The nature of neural invasion by pancreatic cancer [J]. Pancreas, 2007, 35(3): 218223.
11. Beger HG, Rau B, Gansauge F, et al. Treatment of pancreatic cancer: challenge of the facts [J]. World J Surg, 2003, 27(10): 10751084.
12. Dang C, Zhang Y, Ma Q, et al. Expression of nerve growth factor receptors is correlated with progression and prognosis of human pancreatic cancer [J]. J Gastroenterol Hepatol, 2006, 21(5): 850858.
13. Zhu Z, Friess H, diMola FF, et al. Nerve growth factor expression correlates with perineural invasion and pain in human pancreatic cancer [J]. J Clin Oncol, 1999, 17(8): 24192428.
14. di Mola FF, di Sebastiano P. Pain and pain generation in pancreatic cancer [J]. Langenbecks Arch Surg, 2008, 393(6): 919922.
15. Pour PM, Bell RH, Batra SK. Neural invasion in the staging of pancreatic cancer [J]. Pancreas, 2003, 26(4): 322325.
16. Ozaki H, Hiraoka T, Mizumoto R, et al. The prognostic significance of lymph node metastasis and intrapancreatic perineural invasion in pancreatic cancer after curative resection [J]. Surg Today, 1999, 29(1): 1622.
17. Cruveilhier J, Maladies des nerfs. Anatomic Pathologique du Corps Humain [M]. 2nd ed. Paris: J.B. Baillière, 1835: 3335.
18. Ernst P. Uber das Wachstum und die Verbeitung bosartiger Geshwulstte, insbesondere des Krebes in den Lymphbahnen der Nerven [J]. Beitr Path Anat, 1905, 7(Suppl): 2951.
19. Kuwayti K, Baggenstoss AH, Stauffer MH, et al. Carcinoma of the major intrahepatic and the extrahepatic bile ducts exclusive of the papilla of Vater [J]. Surg Gynecol Obstet, 1957, 104(3): 357366.
20. Dunn M, Morgan MB, Beer TW. Perineural invasion: identification, significance, and a standardized definition [J]. Dermatol Surg, 2009, 35(2): 214221.
21. Liebig C, Ayala G, Wilks JA, et al. Perineural invasion in cancer: a review of the literature [J]. Cancer, 2009, 115(15): 33793391.
22. Znker KS, Entschladen F (eds): Neuronal activity in tumor tissue [A]. In: Progression in Experimental Tumor Research [M]. Basel: Karger, 2007: 132133.
23. Eibl G, Reber HA. A xenograft nude mouse model for perineural invasion and recurrence in pancreatic cancer [J]. Pancreas, 2005, 31(3): 258262.
24. Carlson JA, Dickersin GR, Sober AJ, et al. Desmoplastic neurotropic melanoma. A clinicopathologic analysis of 28 cases [J]. Cancer, 1995, 75(2): 478494.
25. Watanabe H, Mizutani T, Haraguchi T, et al. SWI/SNF complex is essential for NRSFmediated suppression of neuronal genes in human nonsmall cell lung carcinoma cell lines [J]. Oncogene, 2006, 25(3): 470479.
26. Chédotal A, Kerjan G, MoreauFauvarque C. The brain within the tumor: new roles for axon guidance molecules in cancers [J]. Cell Death Differ, 2005, 12(8): 10441056.
27. Zhu Z, Kleeff J, Kayed H, et al. Nerve growth factor and enhancement of proliferation, invasion, and tumorigenicity of pancreatic carcinomas cells [J]. Mol Carcinog, 2002, 35(3): 138147.
28. Zhang Y, Dang C, Ma Q, et al. Expression of nerve growth factor receptors and their prognostic value in human pancreatic cancer [J]. Oncol Rep, 2005, 14(1): 161171.
29. Bockman DE, Büchler M, Beger HG. Interaction of pancreatic ductal carcinoma with nerves leads to nerve damage [J]. Gastroenterology, 1994, 107(1): 219230.
30. 郑善川, 梁丽, 张玉茹, 等. GDNF及其受体Ret在腺样囊性癌嗜神经侵袭和细胞增殖中作用的初步研究 [J]. 口腔医学研究, 2010, 26(3): 380383.
31. Ceyhan GO, Giese NA, Erkan M, et al. The neurotrophic factor artemin promotes pancreatic cancer invasion [J]. Ann Surg, 2006, 244(2): 274281.
32. 朱栋良, 罗地来, 罗刚, 等. Artemin、GFRα3在胰腺癌中的表达及其与胰腺癌神经浸润转移的相关性 [J]. 南方医科大学学报, 2009, 29(3): 428431.
33. Ben QW, Wang JC, Liu J, et al. Positive expression of L1CAM is associated with perineural invasion and poor outcome in pancreatic ductal adenocarcinoma [J]. Ann Surg Oncol, 2010, 17(8): 22132221.
34. Farrow B, Albo D, Berger DH. The role of the tumor microenvironment in the progression of pancreatic cancer [J]. J Surg Res, 2008, 149(2): 319328.
35. Ma J, Jiang Y, Jiang Y, et al. Expression of nerve growth factor and tyrosine kinase receptor A and correlation with perineural invasion in pancreatic cancer [J]. J Gastroenterol Hepatol, 2008, 23(12): 18521859.
36. Okada Y, Eibl G, Duffy JP, et al. Glial cellderived neurotrophic factor upregulates the expression and activation of matrix metalloproteinase9 in human pancreatic cancer [J]. Surgery, 2003, 134(2): 293299.
37. Iwahashi N, Nagasaka T, Tezel G, et al. Expression of glial cell linederived neurotrophic factor correlates with perineural invasion of bile duct carcinoma [J]. Cancer, 2002, 94(1): 167174.
38. Podratz JL, Rodriguez E, Windebank AJ. Role of the extracellular matrix in myelination of peripheral nerve [J]. Glia, 2001, 35(1): 3540.
39. Hill RE, Williams RE. A quantitative analysis of perineurial cell basement membrane collagen Ⅳ, laminin and fibronectin in diabetic and nondiabetic human sural nerve [J]. J Anat, 2002, 201(2): 185192.
40. Vega JA, Esteban I, Naves FJ, et al. Immunohistochemical localization of laminin and type Ⅳ collagen in human cutaneous sensory nerve formations [J]. Anat Embryol (Berl), 1995, 191(1): 3339.
41. Ryschich E, Khamidjanov A, Kerkadze V, et al. Promotion of tumor cell migration by extracellular matrix proteins in human pancreatic cancer [J]. Pancreas, 2009, 38(7): 804810.
42. Wang W, Zhao H, Zhang S, et al. Patterns of expression and function of the p75NGFR protein in pancreatic cancer cells and tumours [J]. Eur J Surg Oncol, 2009, 35(8): 826832.
43. Yao J, Ma Q, Wang L, et al. Pleiotrophin expression in human pancreatic cancer and its correlation with clinicopathological features, perineural invasion, and prognosis [J]. Dig Dis Sci, 2009, 54(4): 895901.
44. Abiatari I, DeOliveira T, Kerkadze V, et al. Consensus transcriptome signature of perineural invasion in pancreatic carcinoma [J]. Mol Cancer Ther, 2009, 8(6): 14941504.

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