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[Cancer Research 58, 334-341, January 15, 1998]
© 1998 American Association for Cancer Research
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Frequent Nitric Oxide Synthase-2 Expression in Human Colon Adenomas: Implication for Tumor Angiogenesis and Colon Cancer Progression

Stefan Ambs, William G. Merriam, William P. Bennett, Emanuela Felley-Bosco, Mofolusara O. Ogunfusika, Sean M. Oser, Shawn Klein, Peter G. Shields, Timothy R. Billiar and Curtis C. Harris1

Laboratory of Human Carcinogenesis, National Cancer Institute, NIH, Bethesda, Maryland 20892 [S. A., W. G. M., W. P. B., M. O. O., S. M. O., S. K., P. G. S., C. C. H.]; Institute of Pharmacology and Toxicology, University of Lausanne, CH-1005 Lausanne [E. F.]; and Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania 15261 [T. R. B.]

An increased expression of nitric oxide synthase (NOS) has been observed in human colon carcinoma cell lines as well as in human gynecological, breast, and central nervous system tumors. This observation suggests a pathobiological role of tumor-associated NO production. Hence, we investigated NOS expression in human colon cancer in respect to tumor staging, NOS-expressing cell type(s), nitrotyrosine formation, inflammation, and vascular endothelial growth factor expression. Ca2+-dependent NOS activity was found in normal colon and in tumors but was significantly decreased in adenomas (P < 0.001) and carcinomas (Dukes' stages A–D: P < 0.002). Ca2+-independent NOS activity, indicating inducible NOS (NOS2), is markedly expressed in approximately 60% of human colon adenomas (P < 0.001 versus normal tissues) and in 20–25% of colon carcinomas (P < 0.01 versus normal tissues). Only low levels were found in the surrounding normal tissue. NOS2 activity decreased with increasing tumor stage (Dukes' A–D) and was lowest in colon metastases to liver and lung. NOS2 was detected in tissue mononuclear cells (TMCs), endothelium, and tumor epithelium. There was a statistically significant correlation between NOS2 enzymatic activity and the level of NOS2 protein detected by immunohistochemistry (P < 0.01). Western blot analysis of tumor extracts with Ca2+-independent NOS activity showed up to three distinct NOS2 protein bands at Mr 125,000-Mr 138,000. The same protein bands were heavily tyrosine-phosphorylated in some tumor tissues. TMCs, but not the tumor epithelium, were immunopositive using a polyclonal anti-nitrotyrosine antibody. However, only a subset of the NOS2-expressing TMCs stained positively for 3-nitrotyrosine, which is a marker for peroxynitrite formation. Furthermore, vascular endothelial growth factor expression was detected in adenomas expressing NOS2. These data are consistent with the hypothesis that excessive NO production by NOS2 may contribute to the pathogenesis of colon cancer progression at the transition of colon adenoma to carcinoma in situ.

1 To whom requests for reprints should be addressed, at Laboratory of Human Carcinogenesis, National Cancer Institute, NIH, Building 37/Room 2CO5, 37 Convent Dr., MSC 4255, Bethesda, MD 20892-4255. Phone: (301) 496-2048; Fax: (301) 496-0497; E-mail: Curtis_Harris@nih.gov (E-mail).

Received 7/ 9/97. Accepted 11/12/97.




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A.-C. Souici, J. Mirkovitch, P. Hausel, L. K.Keefer, and E. Felley-Bosco
Transition mutation in codon 248 of the p53 tumor suppressor gene induced by reactive oxygen species and a nitric oxide-releasing compound
Carcinogenesis, February 1, 2000; 21(2): 281 - 287.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
M. Jaiswal, N. F. LaRusso, L. J. Burgart, and G. J. Gores
Inflammatory Cytokines Induce DNA damage and Inhibit DNA repair in Cholangiocarcinoma Cells by a Nitric Oxide-dependent Mechanism
Cancer Res., January 1, 2000; 60(1): 184 - 190.
[Abstract] [Full Text]

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 Exp. Biol. Med.Home page
A. E. Aust and J. F. Eveleigh
Mechanisms of DNA Oxidation
Experimental Biology and Medicine, December 1, 1999; 222(3): 246 - 252.
[Abstract] [Full Text]

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 Am. J. Pathol.Home page
L. C. Jadeski and P. K. Lala
Nitric Oxide Synthase Inhibition by NG-Nitro-L-Arginine Methyl Ester Inhibits Tumor-Induced Angiogenesis in Mammary Tumors
Am. J. Pathol., October 1, 1999; 155(4): 1381 - 1390.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
B. Ahn, B. S. Han, D. J. Kim, and H. Ohshima
Immunohistochemical localization of inducible nitric oxide synthase and 3-nitrotyrosine in rat liver tumors induced by N-nitrosodiethylamine
Carcinogenesis, July 1, 1999; 20(7): 1337 - 1344.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
D. C. GOODWIN, L. M. LANDINO, and L. J. MARNETT
Effects of nitric oxide and nitric oxide-derived species on prostaglandin endoperoxide synthase and prostaglandin biosynthesis
FASEB J, July 1, 1999; 13(10): 1121 - 1136.
[Abstract] [Full Text]

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 Cancer Res.Home page
Q. Shi, S. Huang, W. Jiang, L. S. Kutach, H. N. Ananthaswamy, and K. Xie
Direct Correlation between Nitric Oxide Synthase II Inducibility and Metastatic Ability of UV-2237 Murine Fibrosarcoma Cells Carrying Mutant p53
Cancer Res., May 1, 1999; 59(9): 2072 - 2075.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
C. V. Rao, T. Kawamori, R. Hamid, and B. S. Reddy
Chemoprevention of colonic aberrant crypt foci by an inducible nitric oxide synthase-selective inhibitor
Carcinogenesis, April 1, 1999; 20(4): 641 - 644.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
S. Ambs, W. P. Bennett, W. G. Merriam, M. O. Ogunfusika, S. M. Oser, A. M. Harrington, P. G. Shields, E. Felley-Bosco, S. P. Hussain, and C. C. Harris
Relationship Between p53 Mutations and Inducible Nitric Oxide Synthase Expression in Human Colorectal Cancer
J Natl Cancer Inst, January 6, 1999; 91(1): 86 - 88.
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 Cancer Res.Home page
N. Suh, Y. Wang, T. Honda, G. W. Gribble, E. Dmitrovsky, W. F. Hickey, R. A. Maue, A. E. Place, D. M. Porter, M. J. Spinella, et al.
A Novel Synthetic Oleanane Triterpenoid, 2-Cyano-3,12-dioxoolean-1,9-dien-28-oic Acid, with Potent Differentiating, Antiproliferative, and Anti-Inflammatory Activity
Cancer Res., January 1, 1999; 59(2): 336 - 341.
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 Proc. Natl. Acad. Sci. USAHome page
S. Ambs, M. O. Ogunfusika, W. G. Merriam, W. P. Bennett, T. R. Billiar, and C. C. Harris
Up-regulation of inducible nitric oxide synthase expression in cancer-prone p53 knockout mice
PNAS, July 21, 1998; 95(15): 8823 - 8828.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Rudders, J. Gaspar, R. Madore, C. Voland, F. Grall, A. Patel, A. Pellacani, M. A. Perrella, T. A. Libermann, and P. Oettgen
ESE-1 Is a Novel Transcriptional Mediator of Inflammation That Interacts with NF-kappa B to Regulate the Inducible Nitric-oxide Synthase Gene
J. Biol. Chem., January 26, 2001; 276(5): 3302 - 3309.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
E. Felley-Bosco, F. C. Bender, F. Courjault-Gautier, C. Bron, and A. F. G. Quest
Caveolin-1 down-regulates inducible nitric oxide synthase via the proteasome pathway in human colon carcinoma cells
PNAS, December 19, 2000; 97(26): 14334 - 14339.
[Abstract] [Full Text] [PDF]


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