Research progress of pancreas stellate cells in pancreas fibrosis_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

LONG Dan , ZHOU Yanni , LI Hongsheng , WANG Siqi , LI Lu , ZHANG Jiabi ,  FENG Li ,  LI Shengfu

Key Laboratory of Transplant Engineering and Immunology, Ministry of Health, West China Hospital, Sichuan University, Chengdu 610041, P.R.China;

Corresponding author：

FENG Li, Email: fenglily31@hotmail.com; LI Shengfu, Email: lishengfu@126.com

Keywords：

pancreatitis; pancreas fibrosis; pancreas stellate cell; cell activation

DOI：

10.7507/1007-9424.201609062

Video：

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Objective To review research progress of pancreas stellate cells in pancreas fibrosis and understand characteristics and activation of pancreas stellate cells and its mechanism on pancreas fibrosis. Method The relevant literatures about pancreas stellate cells and its studies in pancreas fibrosis were reviewed. Results The activation of pancreatic stellate cell is associated with fibrosis of pancreatitis and end stage of pancreas transplantation, but its effect and regulation mechanisms for the extracelluar and intracellular molecular network need to be further investigated. Conclusion Elucidation of activation of pancreas stellate cells will facilitate understanding of pancreas fibrosis and searching new target in treatment of pancreas fibrosis.

Citation： LONG Dan, ZHOU Yanni, LI Hongsheng, WANG Siqi, LI Lu, ZHANG Jiabi, FENG Li, LI Shengfu. Research progress of pancreas stellate cells in pancreas fibrosis. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2017, 24(5): 638-643. doi: 10.7507/1007-9424.201609062 Copy

1.	Strobel O, Dadabaeva N, Felix K,et al. Isolation and culture of primary human pancreatic stellate cells that reflect the context of their tissue of origin. Langenbecks Arch Surg, 2016, 401(1): 89-97.
2.	Lee AT, Xu Z, Pothula SP,et al. Alcohol and cigarette smoke components activate human pancreatic stellate cells: implications for the progression of chronic pancreatitis. Alcohol Clin Exp Res, 2015, 39(11): 2123-2133.
3.	Watari N, Hotta Y, Mabuchi Y. Morphological studies on a vitamin A-storing cell and its complex with macrophage observed in mouse pancreatic tissues following excess vitamin A administration. Okajimas Folia Anat Jpn, 1982, 58(4-6): 837-858.
4.	Buchholz M, Kestler HA, Holzmann K,et al. Transcriptome analysis of human hepatic and pancreatic stellate cells: organ-specific variations of a common transcriptional phenotype. J Mol Med (Berl), 2005, 83(10): 795-805.
5.	Mutoh K, Wakuri H, Bo L,et al. Intercalated duct cells in the chicken pancreatic islet. Okajimas Folia Anat Jpn, 1997, 74(4): 147-153.
6.	Bachem MG, Schneider E, Gross H,et al. Identification, culture, and characterization of pancreatic stellate cells in rats and humans. Gastroenterology, 1998, 115(2): 421-432.
7.	Rosendahl AH, Gundewar C, Said Hilmersson K,et al. Conditionally immortalized human pancreatic stellate cell lines demonstrate enhanced proliferation and migration in response to IGF-I. Exp Cell Res, 2015, 330(2): 300-310.
8.	Siegmund SV, Schlosser M, Schildberg FA,et al. Serum amyloid A induces inflammation, proliferation and cell death in activated hepatic stellate cells. PLoS One, 2016, 11(3): e0150893.
9.	Paulo JA, Kadiyala V, Banks PA,et al. Mass spectrometry-based quantitative proteomic profiling of human pancreatic and hepatic stellate cell lines. Genomics Proteomics Bioinformatics, 2013, 11(2): 105-113.
10.	Lee JI, Paik YH, Lee KS,et al. A peroxisome-proliferator activated receptor-gamma ligand could regulate the expression of leptin receptor on human hepatic stellate cells. Histochem Cell Biol, 2007, 127(5): 495-502.
11.	Xiao W, Jiang W, Shen J,et al. Retinoic acid ameliorates pancreatic fibrosis and inhibits the activation of pancreatic stellate cells in mice with experimental chronic pancreatitis via suppressing the Wnt/β-catenin signaling pathway. PLoS One, 2015, 10(11): e0141462.
12.	Yang L, Shen J, He S,et al. L-cysteine administration attenuates pancreatic fibrosis induced by TNBS in rats by inhibiting the activation of pancreatic stellate cell. PLoS One, 2012, 7(2): e31807.
13.	Niina Y, Ito T, Oono T,et al. A sustained prostacyclin analog, ONO-1301, attenuates pancreatic fibrosis in experimental chronic pancreatitis induced by dibutyltin dichloride in rats. Pancreatology, 2014, 14(3): 201-210.
14.	Vogelmann R, Ruf D, Wagner M,et al. Effects of fibrogenic mediators on the development of pancreatic fibrosis in a TGF-beta1 transgenic mouse model. Am J Physiol Gastrointest Liver Physiol, 2001, 280(1): G164-G172.
15.	Haber PS, Keogh GW, Apte MV,et al. Activation of pancreatic stellate cells in human and experimental pancreatic fibrosis. Am J Pathol, 1999, 155(4): 1087-1095.
16.	Yamao J, Toyokawa H, Kim S,et al. Activation of alpha-smooth muscle actin-positive myofibroblast-like cells after chemotherapy with gemcitabine in a rat orthotopic pancreatic cancer model. J Hepatobiliary Pancreat Sci, 2013, 20(2): 206-213.
17.	Gao X, Cao Y, Yang W,et al. BMP2 inhibits TGF-β-induced pancreatic stellate cell activation and extracellular matrix formation. Am J Physiol Gastrointest Liver Physiol, 2013, 304(9): G804-G813.
18.	Shimizu K. Pancreatic stellate cells: molecular mechanism of pancreatic fibrosis. J Gastroenterol Hepatol, 2008, 23 Suppl 1: S119-S121.
19.	Ishiwata T, Kornmann M, Beger HG,et al. Enhanced fibroblast growth factor 5 expression in stromal and exocrine elements of the pancreas in chronic pancreatitis. Gut, 1998, 43(1): 134-139.
20.	Luttenberger T, Schmid-Kotsas A, Menke A,et al. Platelet-derived growth factors stimulate proliferation and extracellular matrix synthesis of pancreatic stellate cells: implications in pathogenesis of pancreas fibrosis. Lab Invest, 2000, 80(1): 47-55.
21.	Masamune A, Satoh A, Watanabe T,et al. Effects of ethanol and its metabolites on human pancreatic stellate cells. Dig Dis Sci, 2010, 55(1): 204-211.
22.	Xu S, Chheda C, Ouhaddi Y,et al. Characterization of mouse models of early pancreatic lesions induced by alcohol and chronic pancreatitis. Pancreas, 2015, 44(6): 882-887.
23.	Schwer CI, Mutschler M, Stoll P,et al. Carbon monoxide releasing molecule-2 inhibits pancreatic stellate cell proliferation by activating p38 mitogen-activated protein kinase/heme oxygenase-1 signaling. Mol Pharmacol, 2010, 77(4): 660-669.
24.	Gryshchenko O, Gerasimenko JV, Gerasimenko OV,et al. Calcium signalling in pancreatic stellate cells: Mechanisms and potential roles. Cell Calcium, 2016, 59(2-3): 140-144.
25.	Pomianowska E, Sandnes D, Grzyb K,et al. Inhibitory effects of prostaglandin E2 on collagen synthesis and cell proliferation in human stellate cells from pancreatic head adenocarcinoma. BMC Cancer, 2014, 14: 413.
26.	Santofimia-Castaño P, Garcia-Sanchez L, Ruy DC,et al. Melatonin induces calcium mobilization and influences cell proliferation independently of MT1/MT2 receptor activation in rat pancreatic stellate cells. Cell Biol Toxicol, 2015, 31(2): 95-110.
27.	Hou XJ, Jin ZD, Jiang F,et al. Expression of Smad7 and Smad ubiquitin regulatory factor 2 in a rat model of chronic pancreatitis. J Dig Dis, 2015, 16(7): 408-415.
28.	Bian K, Zhang F, Wang T,et al. S-adenosylmethionine suppresses the expression of Smad3/4 in activated human hepatic stellate cells via Rac1 promoter methylation. Mol Med Rep, 2016, 13(5): 3867-3873.
29.	Kruse ML, Hopf-Jensen S, Timke C,et al. Differentiation potential of pancreatic fibroblastoid cells/stellate cells: effects of peroxisome proliferator-activated receptor gamma ligands. Int J Cell Biol, 2011, 2011: 816791.
30.	van Westerloo DJ, Florquin S, de Boer AM,et al. Therapeutic effects of troglitazone in experimental chronic pancreatitis in mice. Am J Pathol, 2005, 166(3): 721-728.
31.	Saile B, Knittel T, Matthes N,et al. CD95/CD95L-mediated apoptosis of the hepatic stellate cell. A mechanism terminating uncontrolled hepatic stellate cell proliferation during hepatic tissue repair. Am J Pathol, 1997, 151(5): 1265-1272.
32.	Liu H, Li J, Huang Y,et al. Inhibition of transient receptor potential melastain 7 channel increases HSCs apoptosis induced by TRAIL. Life Sci, 2012, 90(15-16): 612-618.
33.	Hasel C, Dürr S, Rau B,et al. In chronic pancreatitis, widespread emergence of TRAIL receptors in epithelia coincides with neoexpression of TRAIL by pancreatic stellate cells of early fibrotic areas. Lab Invest, 2003, 83(6): 825-836.
34.	Xu P, Zhang Y, Liu Y,et al. Fibroblast growth factor 21 attenuates hepatic fibrogenesis through TGF-β/smad2/3 and NF-κB signaling pathways. Toxicol Appl Pharmacol, 2016, 290: 43-53.
35.	Kim HG, Han JM, Lee JS,et al. Ethyl acetate fraction of Amomum xanthioides improves bile duct ligation-induced liver fibrosis of rat model via modulation of pro-fibrogenic cytokines. Sci Rep, 2015, 5: 14531.
36.	Wu X, Zhang F, Xiong X,et al. Tetramethylpyrazine reduces inflammation in liver fibrosis and inhibits inflammatory cytokine expression in hepatic stellate cells by modulating NLRP3 inflammasome pathway. IUBMB Life, 2015, 67(4): 312-321.
37.	Lin X, Kong LN, Huang C,et al. Hesperetin derivative-7 inhibits PDGF-BB-induced hepatic stellate cell activation and proliferation by targeting Wnt/β-catenin pathway. Int Immunopharmacol, 2015, 25(2): 311-320.
38.	Perera MT, Shimoda M, Kato M,et al. Life-threatening bleeding from duodenal varices due to pancreatic arterio-venous malformation: role of emergency pancreatoduodenectomy. Hepatogastroenterology, 2008, 55(86-87): 1553-1556.
39.	Phillips PA, McCarroll JA, Park S,et al. Rat pancreatic stellate cells secrete matrix metalloproteinases: implications for extracellular matrix turnover. Gut, 2003, 52(2): 275-282.
40.	Lee BJ, Lee HS, Kim CD,et al. The effects of combined treatment with an HMG-CoA reductase inhibitor and PPARγ agonist on the activation of rat pancreatic stellate cells. Gut Liver, 2012, 6(2): 262-269.
41.	刘续宝. 慢性胰腺炎的诊断和治疗. 中国普外基础与临床杂志, 2007, 14(4): 385-387.
42.	Apte MV, Haber PS, Applegate TL,et al. Periacinar stellate shaped cells in rat pancreas: identification, isolation, and culture. Gut, 1998, 43(1): 128-133.

1. Strobel O, Dadabaeva N, Felix K,et al. Isolation and culture of primary human pancreatic stellate cells that reflect the context of their tissue of origin. Langenbecks Arch Surg, 2016, 401(1): 89-97.
2. Lee AT, Xu Z, Pothula SP,et al. Alcohol and cigarette smoke components activate human pancreatic stellate cells: implications for the progression of chronic pancreatitis. Alcohol Clin Exp Res, 2015, 39(11): 2123-2133.
3. Watari N, Hotta Y, Mabuchi Y. Morphological studies on a vitamin A-storing cell and its complex with macrophage observed in mouse pancreatic tissues following excess vitamin A administration. Okajimas Folia Anat Jpn, 1982, 58(4-6): 837-858.
4. Buchholz M, Kestler HA, Holzmann K,et al. Transcriptome analysis of human hepatic and pancreatic stellate cells: organ-specific variations of a common transcriptional phenotype. J Mol Med (Berl), 2005, 83(10): 795-805.
5. Mutoh K, Wakuri H, Bo L,et al. Intercalated duct cells in the chicken pancreatic islet. Okajimas Folia Anat Jpn, 1997, 74(4): 147-153.
6. Bachem MG, Schneider E, Gross H,et al. Identification, culture, and characterization of pancreatic stellate cells in rats and humans. Gastroenterology, 1998, 115(2): 421-432.
7. Rosendahl AH, Gundewar C, Said Hilmersson K,et al. Conditionally immortalized human pancreatic stellate cell lines demonstrate enhanced proliferation and migration in response to IGF-I. Exp Cell Res, 2015, 330(2): 300-310.
8. Siegmund SV, Schlosser M, Schildberg FA,et al. Serum amyloid A induces inflammation, proliferation and cell death in activated hepatic stellate cells. PLoS One, 2016, 11(3): e0150893.
9. Paulo JA, Kadiyala V, Banks PA,et al. Mass spectrometry-based quantitative proteomic profiling of human pancreatic and hepatic stellate cell lines. Genomics Proteomics Bioinformatics, 2013, 11(2): 105-113.
10. Lee JI, Paik YH, Lee KS,et al. A peroxisome-proliferator activated receptor-gamma ligand could regulate the expression of leptin receptor on human hepatic stellate cells. Histochem Cell Biol, 2007, 127(5): 495-502.
11. Xiao W, Jiang W, Shen J,et al. Retinoic acid ameliorates pancreatic fibrosis and inhibits the activation of pancreatic stellate cells in mice with experimental chronic pancreatitis via suppressing the Wnt/β-catenin signaling pathway. PLoS One, 2015, 10(11): e0141462.
12. Yang L, Shen J, He S,et al. L-cysteine administration attenuates pancreatic fibrosis induced by TNBS in rats by inhibiting the activation of pancreatic stellate cell. PLoS One, 2012, 7(2): e31807.
13. Niina Y, Ito T, Oono T,et al. A sustained prostacyclin analog, ONO-1301, attenuates pancreatic fibrosis in experimental chronic pancreatitis induced by dibutyltin dichloride in rats. Pancreatology, 2014, 14(3): 201-210.
14. Vogelmann R, Ruf D, Wagner M,et al. Effects of fibrogenic mediators on the development of pancreatic fibrosis in a TGF-beta1 transgenic mouse model. Am J Physiol Gastrointest Liver Physiol, 2001, 280(1): G164-G172.
15. Haber PS, Keogh GW, Apte MV,et al. Activation of pancreatic stellate cells in human and experimental pancreatic fibrosis. Am J Pathol, 1999, 155(4): 1087-1095.
16. Yamao J, Toyokawa H, Kim S,et al. Activation of alpha-smooth muscle actin-positive myofibroblast-like cells after chemotherapy with gemcitabine in a rat orthotopic pancreatic cancer model. J Hepatobiliary Pancreat Sci, 2013, 20(2): 206-213.
17. Gao X, Cao Y, Yang W,et al. BMP2 inhibits TGF-β-induced pancreatic stellate cell activation and extracellular matrix formation. Am J Physiol Gastrointest Liver Physiol, 2013, 304(9): G804-G813.
18. Shimizu K. Pancreatic stellate cells: molecular mechanism of pancreatic fibrosis. J Gastroenterol Hepatol, 2008, 23 Suppl 1: S119-S121.
19. Ishiwata T, Kornmann M, Beger HG,et al. Enhanced fibroblast growth factor 5 expression in stromal and exocrine elements of the pancreas in chronic pancreatitis. Gut, 1998, 43(1): 134-139.
20. Luttenberger T, Schmid-Kotsas A, Menke A,et al. Platelet-derived growth factors stimulate proliferation and extracellular matrix synthesis of pancreatic stellate cells: implications in pathogenesis of pancreas fibrosis. Lab Invest, 2000, 80(1): 47-55.
21. Masamune A, Satoh A, Watanabe T,et al. Effects of ethanol and its metabolites on human pancreatic stellate cells. Dig Dis Sci, 2010, 55(1): 204-211.
22. Xu S, Chheda C, Ouhaddi Y,et al. Characterization of mouse models of early pancreatic lesions induced by alcohol and chronic pancreatitis. Pancreas, 2015, 44(6): 882-887.
23. Schwer CI, Mutschler M, Stoll P,et al. Carbon monoxide releasing molecule-2 inhibits pancreatic stellate cell proliferation by activating p38 mitogen-activated protein kinase/heme oxygenase-1 signaling. Mol Pharmacol, 2010, 77(4): 660-669.
24. Gryshchenko O, Gerasimenko JV, Gerasimenko OV,et al. Calcium signalling in pancreatic stellate cells: Mechanisms and potential roles. Cell Calcium, 2016, 59(2-3): 140-144.
25. Pomianowska E, Sandnes D, Grzyb K,et al. Inhibitory effects of prostaglandin E2 on collagen synthesis and cell proliferation in human stellate cells from pancreatic head adenocarcinoma. BMC Cancer, 2014, 14: 413.
26. Santofimia-Castaño P, Garcia-Sanchez L, Ruy DC,et al. Melatonin induces calcium mobilization and influences cell proliferation independently of MT1/MT2 receptor activation in rat pancreatic stellate cells. Cell Biol Toxicol, 2015, 31(2): 95-110.
27. Hou XJ, Jin ZD, Jiang F,et al. Expression of Smad7 and Smad ubiquitin regulatory factor 2 in a rat model of chronic pancreatitis. J Dig Dis, 2015, 16(7): 408-415.
28. Bian K, Zhang F, Wang T,et al. S-adenosylmethionine suppresses the expression of Smad3/4 in activated human hepatic stellate cells via Rac1 promoter methylation. Mol Med Rep, 2016, 13(5): 3867-3873.
29. Kruse ML, Hopf-Jensen S, Timke C,et al. Differentiation potential of pancreatic fibroblastoid cells/stellate cells: effects of peroxisome proliferator-activated receptor gamma ligands. Int J Cell Biol, 2011, 2011: 816791.
30. van Westerloo DJ, Florquin S, de Boer AM,et al. Therapeutic effects of troglitazone in experimental chronic pancreatitis in mice. Am J Pathol, 2005, 166(3): 721-728.
31. Saile B, Knittel T, Matthes N,et al. CD95/CD95L-mediated apoptosis of the hepatic stellate cell. A mechanism terminating uncontrolled hepatic stellate cell proliferation during hepatic tissue repair. Am J Pathol, 1997, 151(5): 1265-1272.
32. Liu H, Li J, Huang Y,et al. Inhibition of transient receptor potential melastain 7 channel increases HSCs apoptosis induced by TRAIL. Life Sci, 2012, 90(15-16): 612-618.
33. Hasel C, Dürr S, Rau B,et al. In chronic pancreatitis, widespread emergence of TRAIL receptors in epithelia coincides with neoexpression of TRAIL by pancreatic stellate cells of early fibrotic areas. Lab Invest, 2003, 83(6): 825-836.
34. Xu P, Zhang Y, Liu Y,et al. Fibroblast growth factor 21 attenuates hepatic fibrogenesis through TGF-β/smad2/3 and NF-κB signaling pathways. Toxicol Appl Pharmacol, 2016, 290: 43-53.
35. Kim HG, Han JM, Lee JS,et al. Ethyl acetate fraction of Amomum xanthioides improves bile duct ligation-induced liver fibrosis of rat model via modulation of pro-fibrogenic cytokines. Sci Rep, 2015, 5: 14531.
36. Wu X, Zhang F, Xiong X,et al. Tetramethylpyrazine reduces inflammation in liver fibrosis and inhibits inflammatory cytokine expression in hepatic stellate cells by modulating NLRP3 inflammasome pathway. IUBMB Life, 2015, 67(4): 312-321.
37. Lin X, Kong LN, Huang C,et al. Hesperetin derivative-7 inhibits PDGF-BB-induced hepatic stellate cell activation and proliferation by targeting Wnt/β-catenin pathway. Int Immunopharmacol, 2015, 25(2): 311-320.
38. Perera MT, Shimoda M, Kato M,et al. Life-threatening bleeding from duodenal varices due to pancreatic arterio-venous malformation: role of emergency pancreatoduodenectomy. Hepatogastroenterology, 2008, 55(86-87): 1553-1556.
39. Phillips PA, McCarroll JA, Park S,et al. Rat pancreatic stellate cells secrete matrix metalloproteinases: implications for extracellular matrix turnover. Gut, 2003, 52(2): 275-282.
40. Lee BJ, Lee HS, Kim CD,et al. The effects of combined treatment with an HMG-CoA reductase inhibitor and PPARγ agonist on the activation of rat pancreatic stellate cells. Gut Liver, 2012, 6(2): 262-269.
41. 刘续宝. 慢性胰腺炎的诊断和治疗. 中国普外基础与临床杂志, 2007, 14(4): 385-387.
42. Apte MV, Haber PS, Applegate TL,et al. Periacinar stellate shaped cells in rat pancreas: identification, isolation, and culture. Gut, 1998, 43(1): 128-133.

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Research progress of pancreas stellate cells in pancreas fibrosis

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