Cooperative effects of aminopeptidase N (CD13) expressed by nonmalignant and cancer cells within the tumor microenvironment

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 5, 2012, Pages 1637-1642

  Guzman Rojas, Liliana ^a   Rangel, Roberto ^a   Salameh, Ahmad ^a   Edwards, Julianna K ^a   Dondossola, Eleonora ^a   Kim, Yun Gon ^b   Saghatelian, Alan ^b   Giordano, Ricardo J ^a,c   Kolonin, Mikhail G ^d   Staquicini, Fernanda I ^a   Koivunen, Erkki ^a   Sidman, Richard L ^e   Arap, Wadih ^a   Pasqualini, Renata ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b HARVARD UNIVERSITY   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF TEXAS   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Lung cancer; Melanoma; Proteolytic activity; ShRNA; Tumorigenesis

Indexed keywords

MICROSOMAL AMINOPEPTIDASE; STROMAL CELL DERIVED FACTOR 1;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER GRAFT; CARCINOGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; HOST CELL; HUMAN; HUMAN CELL; LEWIS CARCINOMA; LUNG METASTASIS; MALE; MELANOMA; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION;

ANIMALS; ANTIGENS, CD13; CELL LINE, TUMOR; LUNG NEOPLASMS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

MUS;

EID: 84863171290     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1120790109     Document Type: Article

References (65)

1. Dixon J, et al. (1994) Expression of aminopeptidase-n (CD 13) in normal tissues and malignant neoplasms of epithelial and lymphoid origin. J Clin Pathol 47:43-47. (Pubitemid 24057748)
2. Stange T, Kettmann U, Holzhausen HJ (1996) Immunoelectron microscopic single and double labelling of aminopeptidase N (CD 13) and dipeptidyl peptidase IV (CD 26). Acta Histochem 98:323-331. (Pubitemid 26291891)
3. Mina-Osorio P (2009) The moonlighting enzyme CD13: Old and new functions to target. Trends Mol Med 9:449-456.
4. Favaloro EJ, Moraitis N, Bradstock K, Koutts J (1990) Co-expression of haemopoietic antigens on vascular endothelial cells: A detailed phenotypic analysis. Br J Haematol 74:385-394. (Pubitemid 20122736)
5. Ashmun RA, Look AT (1990) Metalloprotease activity of CD13/aminopeptidase N on the surface of human myeloid cells. Blood 75:462-469. (Pubitemid 20035279)
6. Razak K, Newland AC (1992) Induction of CD13 expression on fresh myeloid leukaemia: Correlation of CD13 expression with aminopeptidase-N activity. Leuk Res 16: 625-630.
7. Shipp MA, Look AT (1993) Hematopoietic differentiation antigens that are membrane- associated enzymes: Cutting is the key! Blood 82:1052-1070. (Pubitemid 23253976)
8. Bogenrieder T, et al. (1997) Expression and localization of aminopeptidase A, aminopeptidase N, and dipeptidyl peptidase IV in benign and malignant human prostate tissue. Prostate 33:225-232. (Pubitemid 27524700)
9. Kehlen A, Lendeckel U, Dralle H, Langner J, Hoang-Vu C (2003) Biological significance of aminopeptidase N/CD13 in thyroid carcinomas. Cancer Res 63:8500-8506. (Pubitemid 37549507)
10. Röcken C, Licht J, Roessner A, Carl-McGrath S (2005) Canalicular immunostaining of aminopeptidase N (CD13) as a diagnostic marker for hepatocellular carcinoma. J Clin Pathol 58:1069-1075. (Pubitemid 41416057)
11. Terauchi M, et al. (2007) Inhibition of APN/CD13 leads to suppressed progressive potential in ovarian carcinoma cells. BMC Cancer 7:140.
12. Teranishi J, et al. (2008) Evaluation of role of angiotensin III and aminopeptidases in prostate cancer cells. Prostate 68:1666-1673.
13. Ito S, et al. (2009) Stromal aminopeptidase N expression: Correlation with angiogenesis in non-small-cell lung cancer. Gen Thorac Cardiovasc Surg 57:591-598.
14. Di Matteo P, et al. (2011) Enhanced expression of CD13 in vessels of inflammatory and neoplastic tissues. J Histochem Cytochem 59:47-59.
15. Bhagwat SV, et al. (2001) CD13/APN is activated by angiogenic signals and is essential for capillary tube formation. Blood 97:652-659. (Pubitemid 32113397)
16. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: The next generation. Cell 144: 646-674.
17. Ozawa MG, et al. (2008) Beyond receptor expression levels: The relevance of target accessibility in ligand-directed pharmacodelivery systems. Trends Cardiovasc Med 18: 126-132.
18. Pasqualini R, et al. (2000) Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis. Cancer Res 60:722-727. (Pubitemid 30094573)
19. Arap W, Pasqualini R, Ruoslahti E (1998) Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science 279:377-380. (Pubitemid 28063372)
20. Khakoo AY, Sidman RL, Pasqualini R, Arap W (2008) Does the renin-angiotensin system participate in regulation of human vasculogenesis and angiogenesis? Cancer Res 68:9112-9115.
21. Nguyen DX, Bos PD, Massagué J (2009) Metastasis: from dissemination to organspecific colonization. Nat Rev Cancer 9:274-284.
22. Joyce JA, Pollard JW (2009) Microenvironmental regulation of metastasis. Nat Rev Cancer 9:239-252.
23. Rangel R, et al. (2007) Impaired angiogenesis in aminopeptidase N-null mice. Proc Natl Acad Sci USA 104:4588-4593. (Pubitemid 47186269)
24. Nicolson GL, Brunson KW, Fidler IJ (1978) Specificity of arrest, survival, and growth of selected metastatic variant cell lines. Cancer Res 38:4105-4111. (Pubitemid 9060148)
25. van Lamsweerde AL, Henry N, Vaes G (1983) Metastatic heterogeneity of cells from Lewis lung carcinoma. Cancer Res 43:5314-5320. (Pubitemid 14230145)
26. Fujii H, et al. (1995) Human melanoma invasion and metastasis enhancement by high expression of aminopeptidase N/CD13. Clin Exp Metastasis 13:337-344.
27. Fontijn D, et al. (2006) CD13/aminopeptidase N overexpression by basic fibroblast growth factor mediates enhanced invasiveness of 1F6 human melanoma cells. Br J Cancer 94:1627-1636. (Pubitemid 43924925)
28. Luan Y, Xu W (2007) The structure and main functions of aminopeptidase N. Curr Med Chem 14:639-647. (Pubitemid 46477717)
29. Alliot F, Rutin J, Leenen PJM, Pessac B (1999) Pericytes and periendothelial cells of brain parenchyma vessels co-express aminopeptidase N, aminopeptidase A, and nestin. J Neurosci Res 58:367-378. (Pubitemid 29508570)
30. Cowburn AS, et al. (2006) Aminopeptidase N (CD13) regulates tumor necrosis factoralpha- induced apoptosis in human neutrophils. J Biol Chem 281:12458-12467. (Pubitemid 43855332)
31. Jiang Y, et al. (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49. (Pubitemid 34742565)
32. Mund JA, Case J (2011) The role of circulating endothelial progenitor cells in tumor angiogenesis. Curr Stem Cell Res Ther 6:115-121.
33. De Palma M, et al. (2005) Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 8:211-226. (Pubitemid 41317592)
34. Shojaei F, et al. (2007) Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat Biotechnol 25:911-920. (Pubitemid 47236916)
35. Menrad A, Speicher D, Wacker J, Herlyn M (1993) Biochemical and functional characterization of aminopeptidase N expressed by human melanoma cells. Cancer Res 53: 1450-1455. (Pubitemid 23097131)
36. Saiki I, et al. (1993) Role of aminopeptidase N (CD13) in tumor-cell invasion and extracellular matrix degradation. Int J Cancer 54:137-143. (Pubitemid 23137011)
37. Ichimura E, Yamada M, Nishikawa K, Abe F, Nakajima T (2006) Immunohistochemical expression of aminopeptidase N (CD13) in human lung squamous cell carcinomas, with special reference to Bestatin adjuvant therapy. Pathol Int 56:296-300. (Pubitemid 43725397)
38. Tokuhara T, et al. (2006) Clinical significance of aminopeptidase N in non-small cell lung cancer. Clin Cancer Res 12:3971-3978. (Pubitemid 44078082)
39. Ikeda N, et al. (2003) Clinical significance of aminopeptidase N/CD13 expression in human pancreatic carcinoma. Clin Cancer Res 9:1503-1508. (Pubitemid 36418408)
40. Oh Y, et al. (2005) Phenotypic diversity of the lung vasculature in experimental models of metastases. Chest 128(6, Suppl)596S-600S. (Pubitemid 43054147)
41. Haraguchi N, et al. (2010) CD13 is a therapeutic target in human liver cancer stem cells. J Clin Invest 120:3326-3339.
42. Inoi K, et al. (1995) Aminopeptidase inhibitor ubenimex (bestatin) inhibits the growth of human choriocarcinoma in nude mice through its direct cytostatic activity. Anticancer Res 15(5B):2081-2087.
43. Imamura N, Kimura A (2000) Effect of ubenimex (Bestatin) on the cell growth and phenotype of HL-60 and HL-60R cell lines: Up- and down-regulation of CD13/aminopeptidase N. Leuk Lymphoma 37:663-667. (Pubitemid 30219079)
44. Tsukamoto H, et al. (2008) Aminopeptidase N (APN)/CD13 inhibitor, Ubenimex, enhances radiation sensitivity in human cervical cancer. BMC Cancer 8:74.
45. Mathé G (1991) Bestatin, an aminopeptidase inhibitor with a multi-pharmacological function. Biomed Pharmacother 45:49-54.
46. Xu Y, Wellner D, Scheinberg DA (1995) Substance P and bradykinin are natural inhibitors of CD13/aminopeptidase N. Biochem Biophys Res Commun 208:664-674.
47. Fortin JP, et al. (2005) Endogenous aminopeptidase N decreases the potency of peptide agonists and antagonists of the kinin B1 receptors in the rabbit aorta. J Pharmacol Exp Ther 314:1169-1176.
48. Danziger RS (2008) Aminopeptidase N in arterial hypertension. Heart Fail Rev 13: 293-298.
49. Hoffmann T, Faust J, Neubert K, Ansorge S (1993) Dipeptidyl peptidase IV (CD 26) and aminopeptidase N (CD 13) catalyzed hydrolysis of cytokines and peptides with N-terminal cytokine sequences. FEBS Lett 336:61-64. (Pubitemid 23362003)
50. Proost P, et al. (2007) Proteolytic processing of CXCL11 by CD13/aminopeptidase N impairs CXCR3 and CXCR7 binding and signaling and reduces lymphocyte and endothelial cell migration. Blood 110:37-44. (Pubitemid 47026816)
51. Kanayama N, et al. (1995) Inactivation of interleukin-8 by aminopeptidase N (CD13). J Leukoc Biol 57:129-134.
52. Kehlen A, et al. (2001) Increased expression of interleukin-8 and aminopeptidase N by cell-cell contact: Interleukin-8 is resistant to degradation by aminopeptidase N/CD13. Eur Cytokine Netw 12:316-324. (Pubitemid 32530390)
53. Palter SF, Mulayim N, Senturk L, Arici A (2001) Interleukin-8 in the human fallopian tube. J Clin Endocrinol Metab 86:2660-2667. (Pubitemid 32545721)
54. Seli E, Senturk LM, Bahtiyar OM, Kayisli UA, Arici A (2001) Expression of aminopeptidase N in human endometrium and regulation of its activity by estrogen. Fertil Steril 75:1172-1176. (Pubitemid 32522616)
55. Tagore DM, et al. (2009) Peptidase substrates via global peptide profiling. Nat Chem Biol 5:23-25.
56. O'Connell PJ, Gerkis V, d'Apice AJ (1991) Variable O-glycosylation of CD13 (aminopeptidase N). J Biol Chem 266:4593-4597. (Pubitemid 21909398)
57. van Hensbergen Y, et al. (2004) Reduced growth, increased vascular area, and reduced response to cisplatin in CD13-overexpressing human ovarian cancer xenografts. Clin Cancer Res 10:1180-1191.
58. Curnis F, et al. (2002) Differential binding of drugs containing the NGR motif to CD13 isoforms in tumor vessels, epithelia, and myeloid cells. Cancer Res 62:867-874. (Pubitemid 34126966)
59. Curnis F, et al. (2000) Enhancement of tumor necrosis factor á antitumor immunotherapeutic properties by targeted delivery to aminopeptidase N (CD13). Nat Biotechnol 18:1185-1190.
60. Zarovni N, Monaco L, Corti A (2004) Inhibition of tumor growth by intramuscular injection of cDNA encoding tumor necrosis factor alpha coupled to NGR and RGD tumor-homing peptides. Hum Gene Ther 15:373-382. (Pubitemid 38469779)
61. Corti A, Ponzoni M (2004) Tumor vascular targeting with tumor necrosis factor alpha and chemotherapeutic drugs. Ann N Y Acad Sci 1028:104-112. (Pubitemid 40361814)
62. Corti A, Curnis F, Arap W, Pasqualini R (2008) The neovasculature homing motif NGR: More than meets the eye. Blood 112:2628-2635.
63. Corti A, Giovannini M, Belli C, Villa E (2010) Immunomodulatory agents with antivascular activity in the treatment of non-small cell lung cancer: Focus on TLR9 agonist, IMiDS and NGR-TNF. J Oncol, 732680.
64. Marcucci F, Corti A (2011) How to improve exposure of tumor cells to drugs: Promoter drugs increase tumor uptake and penetration of effector drugs. Adv Drug Deliv Rev, in press.
65. Tomayko MM, Reynolds CP (1989) Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 24:148-154. (Pubitemid 19163397)