Lipocalin 2 performs contrasting, location-dependent roles in APCmin tumor initiation and progression

Oncogene

Volumn 32, Issue 10, 2013, Pages 1233-1239

  Reilly, P T ^a   Teo, W L ^a   Low, M J ^a   Amoyo Brion, A A ^a   Dominguez Brauer, C ^b   Elia, A J ^b   Berger, T ^b   Greicius, G ^a   Pettersson, S ^a   Mak, T W ^a,b  

^a DIVISION OF MEDICAL ONCOLOGY   (Singapore)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

24p3; intestinal cancer; iron; NGAL

Indexed keywords

APC PROTEIN; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CARCINOGENICITY; CONTROLLED STUDY; DUODENUM; GENE LOSS; INTESTINE TUMOR; IRON STORAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SMALL INTESTINE TUMOR; TUMOR GROWTH; TUMOR VOLUME;

ACUTE-PHASE PROTEINS; ANIMALS; APOPTOSIS; DISEASE PROGRESSION; FEMALE; GENES, APC; INTESTINAL NEOPLASMS; LIPOCALINS; MALE; MICE; MICE, INBRED C57BL; ONCOGENE PROTEINS;

ANIMALIA;

EID: 84874766439     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.159     Document Type: Article

References (50)

1. Berger T, Cheung CC, Elia AJ, Mak TW. Disruption of the Lcn2 gene in mice suppresses primary mammary tumor formation but does not decrease lung metastasis. Proc Natl Acad Sci USA 2010; 107: 2995-3000.
2. Leng X, Ding T, Lin H, Wang Y, Hu L, Hu J et al. Inhibition of lipocalin 2 impairs breast tumorigenesis and metastasis. Cancer Res 2009; 69: 8579-8584.
3. Friedl A, Stoesz SP, Buckley P, Gould MN. Neutrophil gelatinase- associated lipocalin in normal and neoplastic human tissues. Cell type-specific pattern of expression. Histochem J 1999; 31: 433-441.
4. Stoesz SP, Friedl A, Haag JD, Lindstrom MJ, Clark GM, Gould MN. Heterogeneous expression of the lipocalin NGAL in primary breast cancers. Int J Cancer 1998; 79: 565-572.
5. Bauer M, Eickhoff JC, Gould MN, Mundhenke C, Maass N, Friedl A. Neutrophil gelatinase-associated lipocalin (NGAL) is a predictor of poor prognosis in human primary breast cancer. Breast Cancer Res Treat 2008; 108: 389-397.
6. Fernandez CA, Yan L, Louis G, Yang J, Kutok JL, Moses MA. The matrix metalloproteinase- 9/neutrophil gelatinase-associated lipocalin complex plays a role in breast tumor growth and is present in the urine of breast cancer patients. Clin Cancer Res 2005; 11: 5390-5395.
7. Shen ZZ, Zhao W, Gu J, Zhang ZQ, Yan L. [Expression of matrix metalloproteinase- 9 and its complex in the urine of breast cancer patients]. Zhonghua Wai Ke Za Zhi 2003; 41: 817-819.
8. Alpizar-Alpizar W, Laerum OD, Illemann M, Ramirez JA, Arias A, Malespin-Bendana W et al. Neutrophil gelatinase-associated lipocalin (NGAL/Lcn2) is upregulated in gastric mucosa infected with Helicobacter pylori. Virchows Arch 2009; 455: 225-233.
9. Kubben FJ, Sier CF, Hawinkels LJ, Tschesche H, van Duijn W, Zuidwijk K et al. Clinical evidence for a protective role of lipocalin-2 against MMP-9 autodegradation and the impact for gastric cancer. Eur J Cancer 2007; 43: 1869-1876.
10. Wang HJ, He XJ, Ma YY, Jiang XT, Xia YJ, Ye ZY et al. Expressions of neutrophil gelatinase-associated lipocalin in gastric cancer: a potential biomarker for prognosis and an ancillary diagnostic test. Anat Rec 2010; 293: 1855-1863.
11. Zhang H, Xu L, Xiao D, Xie J, Zeng H, Wang Z et al. Upregulation of neutrophil gelatinase-associated lipocalin in oesophageal squamous cell carcinoma: significant correlation with cell differentiation and tumour invasion. J Clin Pathol 2007; 60: 555-561.
12. Barresi V, Ieni A, Bolignano D, Magno C, Buemi M, Barresi G. Neutrophil gelatinaseassociated lipocalin immunoexpression in renal tumors: correlation with histotype and histological grade. Oncol Rep 2010; 24: 305-310.
13. Barresi V, Tuccari G, Barresi G. NGAL immunohistochemical expression in brain primary and metastatic tumors. Clin Neuropathol 2010; 29: 317-322.
14. Barresi V, Reggiani-Bonetti L, Di Gregorio C, Vitarelli E, Ponz De Leon M, Barresi G. Neutrophil gelatinase-associated lipocalin (NGAL) and matrix metalloproteinase-9 (MMP-9) prognostic value in stage I colorectal carcinoma. Pathol Res Pract 2011; 207: 479-486.
15. Nielsen BS, Borregaard N, Bundgaard JR, Timshel S, Sehested M, Kjeldsen L. Induction of NGAL synthesis in epithelial cells of human colorectal neoplasia and inflammatory bowel diseases. Gut 1996; 38: 414-420.
16. Ryon J, Bendickson L, Nilsen-Hamilton M. High expression in involuting reproductive tissues of uterocalin/24p3, a lipocalin and acute phase protein. Biochem J 2002; 367Pt 1: 271-277.
17. Mori K, Nakao K. Neutrophil gelatinase-associated lipocalin as the real-Time indicator of active kidney damage. Kidney Int 2007; 71: 967-970.
18. Carlson M, Raab Y, Seveus L, Xu S, Hallgren R, Venge P. Human neutrophil lipocalin is a unique marker of neutrophil inflammation in ulcerative colitis and proctitis. Gut 2002; 50: 501-506.
19. Rodvold JJ, Mahadevan NR, Zanetti M. Lipocalin 2 in cancer: when good immunity goes bad. Cancer Lett 2012; 316: 132-138.
20. Yan L, Borregaard N, Kjeldsen L, Moses MA. The high molecular weight urinary matrix metalloproteinase (MMP) activity is a complex of gelatinase B/MMP-9 and neutrophil gelatinase-associated lipocalin (NGAL). Modulation of MMP-9 activity by NGAL. J Biol Chem 2001; 276: 37258-37265.
21. Nuntagowat C, Leelawat K, Tohtong R. NGAL knockdown by siRNA in human cholangiocarcinoma cells suppressed invasion by reducing NGAL/MMP-9 complex formation. Clin Exp Metastasis 2010; 27: 295-305.
22. Bachman MA, Miller VL, Weiser JN. Mucosal lipocalin 2 has pro-inflammatory and iron-sequestering effects in response to bacterial enterobactin. PLoS Pathog 2009; 5: e1000622.
23. Fischbach MA, Lin H, Zhou L, Yu Y, Abergel RJ, Liu DR et al. The pathogenassociated iroA gene cluster mediates bacterial evasion of lipocalin 2. Proc Natl Acad Sci USA 2006; 103: 16502-16507.
24. Flo TH, Smith KD, Sato S, Rodriguez DJ, Holmes MA, Strong RK et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 2004; 432: 917-921.
25. Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN, Strong RK. The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell 2002; 10: 1033-1043.
26. Bao G, Clifton M, Hoette TM, Mori K, Deng SX, Qiu A et al. Iron traffics in circulation bound to a siderocalin (Ngal)-catechol complex. Nat Chem Biol 2010; 6: 602-609.
27. Devireddy LR, Gazin C, Zhu X, Green MR. A cell-surface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. Cell 2005; 123: 1293-1305.
28. Devireddy LR, Hart DO, Goetz DH, Green MR. A mammalian siderophore synthesized by an enzyme with a bacterial homolog involved in enterobactin production. Cell 2010; 141: 1006-1017.
29. Hvidberg V, Jacobsen C, Strong RK, Cowland JB, Moestrup SK, Borregaard N. The endocytic receptor megalin binds the iron transporting neutrophil- gelatinaseassociated lipocalin with high affinity and mediates its cellular uptake. FEBS Lett 2005; 579: 773-777.
30. Yang J, Goetz D, Li JY, Wang W, Mori K, Setlik D et al. An iron delivery pathway mediated by a lipocalin. Mol Cell 2002; 10: 1045-1056.
31. Vinuesa E, Sola A, Jung M, Alfaro V, Hotter G. Lipocalin-2-induced renal regeneration depends on cytokines. Am J Physiol Renal Physiol 2008; 295: F1554-F1562.
32. Zhang J, Wu Y, Zhang Y, Leroith D, Bernlohr DA, Chen X. The role of lipocalin 2 in the regulation of inflammation in adipocytes and macrophages. Mol Endocrinol 2008; 22: 1416-1426.
33. Moser AR, Luongo C, Gould KA, McNeley MK, Shoemaker AR, Dove WF. ApcMin: a mouse model for intestinal and mammary tumorigenesis. Eur J Cancer 1995; 31A: 1061-1064.
34. Rakoff-Nahoum S, Medzhitov R. Regulation of spontaneous intestinal tumorigenesis through the adaptor protein MyD88. Science 2007; 317: 124-127.
35. Dove WF, Clipson L, Gould KA, Luongo C, Marshall DJ, Moser AR et al. Intestinal neoplasia in the ApcMin mouse: independence from the microbial and natural killer (beige locus) status. Cancer Res 1997; 57: 812-814.
36. Li Y, Kundu P, Seow SW, de Matos CT, Aronsson L, Chin KC et al. Gut microbiota accelerate tumor growth via c-jun and STAT3 phosphorylation in APCMin/ mice. Carcinogenesis 2012 (PMID: 22461519).
37. Sinnamon MJ, Carter KJ, Fingleton B, Matrisian LM. Matrix metalloproteinase-9 contributes to intestinal tumourigenesis in the adenomatous polyposis coli multiple intestinal neoplasia mouse. Int J Exp Pathol 2008; 89: 466-475.
38. Wilson CL, Heppner KJ, Labosky PA, Hogan BL, Matrisian LM. Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin. Proc Natl Acad Sci USA 1997; 94: 1402-1407.
39. Rao CV, Yang YM, Swamy MV, Liu T, Fang Y, Mahmood R et al. Colonic tumorigenesis in BubR1/-ApcMin/ compound mutant mice is linked to premature separation of sister chromatids and enhanced genomic instability. Proc Natl Acad Sci USA 2005; 102: 4365-4370.
40. Wang D, Wang H, Shi Q, Katkuri S, Walhi W, Desvergne B et al. Prostaglandin E(2) promotes colorectal adenoma growth via transactivation of the nuclear peroxisome proliferator-activated receptor delta. Cancer Cell 2004; 6: 285-295.
41. Yang J, Bielenberg DR, Rodig SJ, Doiron R, Clifton MC, Kung AL et al. Lipocalin 2 promotes breast cancer progression. Proc Natl Acad Sci USA 2009; 106: 3913-3918.
42. Baltgalvis KA, Berger FG, Pena MM, Davis JM, Carson JA. Effect of exercise on biological pathways in ApcMin/ mouse intestinal polyps. J Appl Physiol 2008; 104: 1137-1143.
43. Hata K, Tanaka T, Kohno H, Suzuki R, Qiang SH, Yamada Y et al. Beta-cateninaccumulated crypts in the colonic mucosa of juvenile ApcMin/ mice. Cancer Lett 2006; 239: 123-128.
44. Mutanen M, Pajari AM, Oikarinen SI. Beef induces and rye bran prevents the formation of intestinal polyps in Apc(Min) mice: relation to beta-catenin and PKC isozymes. Carcinogenesis 2000; 21: 1167-1173.
45. Murphy EA, Davis JM, McClellan JL, Gordon BT, Carmichael MD. Curcumin's effect on intestinal inflammation and tumorigenesis in the ApcMin/ mouse. J Interferon Cytokine Res 2011; 31: 219-226.
46. Xiao H, Yin W, Khan MA, Gulen MF, Zhou H, Sham HP et al. Loss of single immunoglobulin interlukin-1 receptor-related molecule leads to enhanced colonic polyposis in Apc(min) mice. Gastroenterology 2010; 139: 574-585.
47. Dale JC, Burritt MF, Zinsmeister AR. Diurnal variation of serum iron, iron-binding capacity, transferrin saturation, and ferritin levels. Am J Clin Pathol 2002; 117: 802-808.
48. Forbes A. Iron and parenteral nutrition. Gastroenterology 2009; 137: S47-S54.
49. Xu G, Ahn J, Chang S, Eguchi M, Ogier A, Han S et al. Lipocalin-2 induces cardiomyocyte apoptosis by increasing intracellular iron accumulation. J Biol Chem 2011; 287: 4808-4817.
50. Berger T, Togawa A, Duncan GS, Elia AJ, You-Ten A, Wakeham A et al. Lipocalin 2-deficient mice exhibit increased sensitivity to Escherichia coli infection but not to ischemia-reperfusion injury. Proc Natl Acad Sci USA 2006; 103: 1834-1839.