Concurrent PEDF deficiency and Kras mutation induce invasive pancreatic cancer and adipose-rich stroma in mice

Gut

Volumn 61, Issue 10, 2012, Pages 1454-1464

  Grippo, PaulJ ^a   Fitchev, Philip S ^b   Bentrem, David J ^a   Melstrom, Laleh G ^a   Dangi Garimella, Surabhi ^a   Krantz, Seth B ^a   Heiferman, Michael J ^a   Chung, Chuhan ^c   Adrian, Kevin ^a   Cornwell, Mona L ^b   Flesche, Jan B ^d   Rao, Sambasiva M ^a   Talamonti, Mark S ^b   Munshi, Hidayatullah G ^a   Crawford, Susan E ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOPHILIN; GELATINASE A; GELATINASE B; PERILIPIN 2; PERILIPIN 3; PIGMENT EPITHELIUM DERIVED FACTOR; PROTEIN; TAIL INTERACTING PROTEIN 47; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; VASCULOTROPIN;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; CANCER INVASION; CARCINOGENESIS; CELL INFILTRATION; CLINICAL ARTICLE; CONTROLLED STUDY; EL KRAS MOUSE; EMBRYO; GENE MUTATION; HUMAN; HUMAN TISSUE; HYPERTROPHY; LIPID METABOLISM; LIPOLYSIS; MOUSE; MOUSE STRAIN; NONHUMAN; OBESITY; ONCOGENE K RAS; PANCREAS ADENOCARCINOMA; PANCREAS ISLET CELL HYPERPLASIA; PRECANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEATOSIS; STROMA; TISSUE LEVEL; TUMOR MICROENVIRONMENT;

ADIPOCYTES, WHITE; ADIPOSITY; ANIMALS; BLOTTING, WESTERN; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; EYE PROTEINS; GENETIC MARKERS; HUMANS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; MUTATION; NEOPLASM INVASIVENESS; NERVE GROWTH FACTORS; PANCREAS; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS P21(RAS); REAL-TIME POLYMERASE CHAIN REACTION; SERPINS; STROMAL CELLS; TUMOR MARKERS, BIOLOGICAL;

EID: 84866118062     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2011-300821     Document Type: Article

References (48)

1. Calle E, Rodriguez C, Walker-Thurmond K, et al. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med. 2003;348:1625-38. (Pubitemid 36459468)
2. Li D, Morris JS, Liu J, et al. Body mass index and risk, age of onset, and survival in patients with pancreatic cancer. JAMA 2009;301:2553-62.
3. Giovannucci E, Michaud D. The role of obesity and related metabolic disturbances in cancers of the colon, prostate, and pancreas. Gastroenterology 2007;132:2208-25. (Pubitemid 46693749)
4. Mathur A, Zyromski NJ, Pitt HA, et al. Pancreatic steatosis promotes dissemination and lethality of pancreatic cancer. J Am Coll Surg 2009;208:989-94.
5. Zyromski NJ, Mathur A, Pitt HA, et al. Obesity potentiates the growth and dissemination of pancreatic cancer. Surgery 2009;146:258-63.
6. Koska J, Stefan N, Permana PA, et al. Increased fat accumulation in liver may link insulin resistance with subcutaneous abdominal adipocyte enlargement, visceral adiposity, and hypoadiponectinemia in obese individuals. Am J Clin Nutr 2008;87:295-302.
7. Brasaemle DL. Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J Lipid Res 2007;48:2547-59. (Pubitemid 350272839)
8. Bickel PE, Tansey JT, Welte MA. PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. Biochim Biophys Acta 2009;1791:419-40.
9. Zechner R, Kienesberger PC, Haemmerle G, et al. Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J Lipid Res 2009;50:3-21.
10. Straub BK, Herpel E, Singer S, et al. Lipid droplet-associated PAT-proteins show frequent and differential expression in neoplastic steatogenesis. Mod Pathol 2010;23:480-92.
11. Steele FR, Chader GJ, Johnson LV, et al. Pigment epithelium-derived factor: neurotrophic activity and identification as a member of the serine protease inhibitor gene family. Proc Natl Acad Sci U S A 1993;90:1526-30. (Pubitemid 23058206)
12. Broadhead ML, Dass CR, Choong PF. Cancer cell apoptotic pathways mediated by PEDF: prospects for therapy. Trends Mol Med 2009;15:461-7.
13. Dawson DW, Volpert OV, Gillis P, et al. Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science 1999;285:245-8. (Pubitemid 29329995)
14. Crawford SE, Stellmach V, Ranalli M, et al. Pigment epithelium-derived factor (PEDF) in neuroblastoma: a multifunctional mediator of Schwann cell antitumor activity. J Cell Sci 2001;114:4421-8. (Pubitemid 34082862)
15. Yamagishi SI, Matsui T, Adachi H, et al. Positive association of circulating levels of advanced glycation end products (AGEs) with pigment epithelium-derived factor (PEDF) in a general population. Pharmacol Res 2019;61:103-7.
16. Yoshida T, Yamagishi S, Nakamura K, et al. Pigment epithelium-derived factor (PEDF) ameliorates advanced glycation end product (AGE)-induced hepatic insulin resistance in vitro by suppressing Rac-1 activation. Horm Metab Res 2008;40:620-5.
17. Crowe S, Wu LE, Economou C, et al. Pigment epithelium-derived factor contributes to insulin resistance in obesity. Cell Metab 2009;10:40-7.
18. Chung C, Doll JA, Gattu AK, et al. Anti-angiogenic pigment epithelium-derived factor regulates hepatocyte triglyceride content through adipose triglyceride lipase (ATGL). J Hepatol 2008;48:471-8.
19. Doll JA, Stellmach VM, Bouck NP, et al. Pigment epithelium-derived factor regulates the vasculature and mass of the prostate and pancreas. Nat Med 2003;9:774-80. (Pubitemid 36749229)
20. Cai J, Parr C, Watkins G, et al. Decreased pigment epithelium-derived factor expression in human breast cancer progression. Clin Cancer Res 2006;12:3510-17.
21. Uehara H, Miyamoto M, Kato K, et al. Expression of pigment epithelium-derived factor decreases liver metastasis and correlates with favorable prognosis for patients with ductal pancreatic adenocarcinoma. Cancer Res 2004;64:3533-7. (Pubitemid 38657928)
22. Hase R, Miyamoto M, Uehara H, et al. Pigment epithelium-derived factor gene therapy inhibits human pancreatic cancer in mice. Clin Cancer Res 2005;11:8737-44. (Pubitemid 43005924)
23. Benito M, Porras A, Nebreda AR, et al. Differentiation of 3T3-L1 fibroblasts to adipocytes induced by transfection of ras oncogenes. Science 1991;253:565-8. (Pubitemid 21917190)
24. Grippo PJ, Nowlin PS, Demeure MJ, et al. Preinvasive pancreatic neoplasia of ductal phenotype induced by acinar cell targeting of mutant Kras in transgenic mice. Cancer Res 2003;63:2016-19. (Pubitemid 36538599)
25. Jamieson N, Foulis A, Oien K, et al. Peripancreatic fat invasion is an independent predictor of poor outcome following pancreaticoduodenectomy for pancreatic ductal adenocarcinoma. J Gastrointest Surgery 2011;15:512-24.
26. Ottaviano AJ, Sun L, Ananthanarayanan V, et al. Extracellular matrix-mediated membrane-type 1 matrix metalloproteinase expression in pancreatic ductal cells is regulated by transforming growth factor-beta1. Cancer Res 2006;66:7032-40. (Pubitemid 44197679)
27. Shields MA, Dangi-Garimella S, Krantz SB, et al. Pancreatic cancer cells respond to type I collagen by inducing snail expression to promote membrane type 1 matrix metalloproteinase-dependent collagen invasion. J Biol Chem 2011;286:10495-504.
28. Joseph MJ, Dangi-Garimella S, Shields MA, et al. Slug is a downstream mediator of transforming growth factor-beta1-induced matrix metalloproteinase-9 expression and invasion of oral cancer cells. J Cell Biochem 2009;108:726-36.
29. Esposito I, Seiler C, Bergmann F, et al. Hypothetical progression model of pancreatic cancer with origin in the centroacinar-acinar compartment. Pancreas 2007;35:212-17. (Pubitemid 47482512)
30. Gao G, Li Y, Zhang D, et al. Unbalanced expression of VEGF and PEDF in ischemia-induced retinal neovascularization. FEBS Lett 2001;489:270-6. (Pubitemid 32126422)
31. Zheng Z, Chen H, Ke G, et al. Protective effect of perindopril on diabetic retinopathy is associated with decreased vascular endothelial growth factor-to-pigment epithelium-derived factor ratio: involvement of a mitochondria-reactive oxygen species pathway. Diabetes 2009;58:954-64.
32. Filleur S, Nelius T, de Riese W, et al. Characterization of PEDF: a multi-functional serpin family protein. J Cell Biochem 2009;106:769-75.
33. Londos C, Sztalryd C, Tansey JT, et al. Role of PAT proteins in lipid metabolism. Biochimie 2005;87:45-9. (Pubitemid 40305232)
34. Sztalryd C, Bell M, Lu X, et al. Functional compensation for adipose differentiation-related protein (ADFP) by Tip47 in an ADFP null embryonic cell line. J Biol Chem 2006;281:34341-8. (Pubitemid 46043256)
35. Blüher M. Adipose tissue dysfunction in obesity. Exp Clin Endocrinol Diabetes 2009;117:241-50.
36. Anand SS, Tarnopolsky MA, Rashid S, et al. Factors in South Asians: the molecular study of health and risk in ethnic groups (mol-SHARE). PLoS One 2011;6:e22112.
37. Veilleux A, Caron-Jobin M, Noël S, et al. Visceral adipocyte hypertrophy is associated with dyslipidemia independent of body composition and fat distribution in women. Diabetes 2011;60:1504-11.
38. Blüher M, Wilson-Fritch L, Leszyk J, et al. Role of insulin action and cell size on protein expression patterns in adipocytes. J Biol Chem 2004;279:31902-9.
39. Bost F, Aouadi M, Caron L, et al. The role of MAPKs in adipocyte differentiation and obesity. Biochimie 2005;87:51-6. (Pubitemid 40298765)
40. Wang M, Wang JJ, Li J, et al. Pigment epithelium-derived factor suppresses adipogenesis via inhibition of the MAPK/ERK pathway in 3T3-L1 preadipocytes. Am J Physiol Endocrinol Metab 2009;297:E1378-87.
41. Hruban RH, Adsay NV, Albores-Saavedra J, et al. Pathology of genetically engineered mouse models of pancreatic exocrine cancer: consensus report and recommendations. Cancer Res 2006;66:95-106. (Pubitemid 43166014)
42. Colby JK, Klein RD, McArthur MJ, et al. Progressive metaplastic and dysplastic changes in mouse pancreas induced by cyclooxygenase-2 overexpression. Neoplasia 2008;10:782-96.
43. Wagner M, Greten FR, Weber CK, et al. A murine tumour progression model for pancreatic cancer recapitulating the genetic alterations of the human disease. Genes Dev 2001;15:286-93. (Pubitemid 32155144)
44. Bergers G, Brekken R, McMahon G, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000;2:737-44.
45. Notari L, Miller A, Martínez A, et al. Pigment epithelium-derived factor is a substrate for matrix metalloproteinase type 2 and type 9: implications for downregulation in hypoxia. Invest Ophthalmol Vis Sci 2005;46:2736-47. (Pubitemid 43086693)
46. Croissandeau G, Chrétien M, Mbikay M. Involvement of matrix metalloproteinases in the adipose conversion of 3T3-L1 preadipocytes. Biochem J 2002;364:739-46. (Pubitemid 34680850)
47. Derosa G, Ferrari I, D'Angelo A, et al. Matrix metalloproteinase-2 and -9 levels in obese patients. Endothelium 2008;15:219-24.
48. Catalán V, Gómez-Ambrosi J, Rodríguez A, et al. Increased adipose tissue expression of lipocalin-2 in obesity is related to inflammation and matrix metalloproteinase-2 and metalloproteinase-9 activities in humans. J Mol Med. 2009;87:803-13.