Reduced susceptibility to azoxymethane-induced aberrant crypt foci formation and colon cancer in growth hormone deficient rats

Growth Hormone and IGF Research

Volumn 19, Issue 5, 2009, Pages 447-456

  Carroll, Robert E ^a,e   Goodlad, Robert A ^b   Poole, Aleksandra J ^a   Tyner, Angela L ^a   Robey, R Brooks ^c,d   Swanson, Steven M ^a   Unterman, Terry G ^a,e  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

^d VA MEDICAL CENTER   (United States)

^e Jesse Brown Veterans Affairs Medical Center   (United States)

Author keywords

Aberrant crypt foci; Azoxymethane; Carcinogenesis; Growth hormone

Indexed keywords

AZOXYMETHANE; BROXURIDINE; CASPASE 3; CYCLIN DEPENDENT KINASE INHIBITOR 1B; GROWTH HORMONE; HEXOKINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; VINCRISTINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL PROLIFERATION; COLON CANCER; COLON CARCINOGENESIS; CONTROLLED STUDY; DWARFISM; ENZYME ACTIVITY; FLOW CYTOMETRY; GENOTYPE; GROWTH HORMONE DEFICIENCY; IMMUNOHISTOCHEMISTRY; INTESTINE CRYPT; MALE; METAPHASE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOIMMUNOASSAY; RAT; SPECTROPHOTOMETRY; STEREOMICROSCOPY; WESTERN BLOTTING; WILD TYPE;

ANIMALS; APOPTOSIS; AZOXYMETHANE; CARCINOGENS; COLON; COLONIC NEOPLASMS; DISEASE SUSCEPTIBILITY; GROWTH HORMONE; MALE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 70349466552     PISSN: 10966374     EISSN: 15322238     Source Type: Journal    
DOI: 10.1016/j.ghir.2009.02.001     Document Type: Article

References (72)

1. Lann D., and LeRoith D. The role of endocrine insulin-like growth factor-I and insulin in breast cancer. J. Mammary Gland Biol. Neoplasia 13 (2008) 371-379
2. Nam R.K., Trachtenberg J., Jewett M.A., Toi A., Evans A., Emami M., Narod S.A., and Pollak M. Serum insulin-like growth factor-I levels and prostatic intraepithelial neoplasia: a clue to the relationship between IGF-I physiology and prostate cancer risk. Cancer Epidemiol. Biomarkers Prev. 14 (2005) 1270-1273
3. Giovannucci E. Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J. Nutr. 131 (2001) 3109S-3120S
4. Samani A.A., Yakar S., LeRoith D., and Brodt P. The role of the IGF system in cancer growth and metastasis: overview and recent insights. Endocr. Rev. 28 (2007) 20-47
5. Jenkins P.J., Frajese V., Jones A.M., Camacho-Hubner C., Lowe D.G., Fairclough P.D., Chew S.L., Grossman A.B., Monson J.P., and Besser G.M. Insulin-like growth factor I and the development of colorectal neoplasia in acromegaly. J. Clin. Endocrinol. Metab. 85 (2000) 3218-3221
6. Matano Y., Okada T., Suzuki A., Yoneda T., Takeda Y., and Mabuchi H. Risk of colorectal neoplasm in patients with acromegaly and its relationship with serum growth hormone levels. Am. J. Gastroenterol. 100 (2005) 1154-1160
7. Le Marchand L., Donlon T., Seifried A., Kaaks R., Rinaldi S., and Wilkens L.R. Association of a common polymorphism in the human GH1 gene with colorectal neoplasia. J. Natl. Cancer Inst. 94 (2002) 454-460
8. Schoen R.E., Weissfeld J.L., Kuller L.H., Thaete F.L., Evans R.W., Hayes R.B., and Rosen C.J. Insulin-like growth factor-I and insulin are associated with the presence and advancement of adenomatous polyps. Gastroenterology 129 (2005) 464-475
9. Saydah S.H., Platz E.A., Rifai N., Pollak M.N., Brancati F.L., and Helzlsouer K.J. Association of markers of insulin and glucose control with subsequent colorectal cancer risk. Cancer Epidemiol. Biomarkers Prev. 12 (2003) 412-418
10. Nomura A.M., Stemmermann G.N., Lee J., and Pollak M.N. Serum insulin-like growth factor I and subsequent risk of colorectal cancer among Japanese-American men. Am. J. Epidemiol. 158 (2003) 424-431
11. Gargosky S.E., Nanto-Salonen K., Tapanainen P., and Rosenfeld R.G. Pregnancy in growth hormone-deficient rats: assessment of insulin-like growth factors (IGFs), IGF-binding proteins (IGFBPs) and IGFBP protease activity. J. Endocrinol. 136 (1993) 479-489
12. Okuma S. Study of growth hormone in spontaneous dwarf rat. Nippon Naibunpi Gakkai Zasshi 60 (1984) 1005-1014
13. Takeuchi T., Suzuki H., Sakurai S., Nogami H., Okuma S., and Ishikawa H. Molecular mechanism of growth hormone (GH) deficiency in the spontaneous dwarf rat: detection of abnormal splicing of GH messenger ribonucleic acid by the polymerase chain reaction. Endocrinology 126 (1990) 31-38
14. Sonntag W.E., Carter C.S., Ikeno Y., Ekenstedt K., Carlson C.S., Loeser R.F., Chakrabarty S., Lee S., Bennett C., Ingram R., Moore T., and Ramsey M. Adult-onset growth hormone and insulin-like growth factor I deficiency reduces neoplastic disease, modifies age-related pathology, and increases life span. Endocrinology 146 (2005) 2920-2932
15. Dipple A. DNA adducts of chemical carcinogens. Carcinogenesis 16 (1995) 437-441
16. Bird R.P. Observation and quantification of aberrant crypts in the murine colon treated with a colon carcinogen: preliminary findings. Cancer Lett. 37 (1987) 147-151
17. Hirose Y., Yoshimi N., Makita H., Hara A., Tanaka T., and Mori H. Early alterations of apoptosis and cell proliferation in azoxymethane-initiated rat colonic epithelium. Jpn. J. Cancer Res. 87 (1996) 575-582
18. Ponder B.A., and Wilkinson M.M. Direct examination of the clonality of carcinogen-induced colonic epithelial dysplasia in chimeric mice. J. Natl. Cancer Inst. 77 (1986) 967-976
19. Siu I.M., Robinson D.R., Schwartz S., Kung H.J., Pretlow T.G., Petersen R.B., and Pretlow T.P. The identification of monoclonality in human aberrant crypt foci. Cancer Res. 59 (1999) 63-66
20. Park H.S., Goodlad R.A., and Wright N.A. Crypt fission in the small intestine and colon. A mechanism for the emergence of G6PD locus-mutated crypts after treatment with mutagens. Am. J. Pathol. 147 (1995) 1416-1427
21. Kristt D., Bryan K., and Gal R. Colonic aberrant crypts may originate from impaired fissioning: relevance to increased risk of neoplasia. Hum. Pathol. 30 (1999) 1449-1458
22. Nogami H., Tachibana T., and Ishikawa H. Intrauterine growth retardation due to growth hormone deficiency in rats. Biol. Neonate 68 (1995) 412-418
23. McLellan E.A., and Bird R.P. Aberrant crypts: potential preneoplastic lesions in the murine colon. Cancer Res. 48 (1988) 6187-6192
24. E.B. Prophet, Armed Forces Institute of Pathology (US) and American Registry of Pathology, Laboratory Methods in Histotechnology. American Registry of Pathology, Washington, DC, 1994.
25. Alferez D., and Goodlad R.A. To best measure cell proliferation in samples from the intestine. Cell Prolif. 40 (2007) 231-240
26. Weidner N., Moore II D.H., Ljung B.M., Waldman F.M., Goodson III W.H., Mayall B., Chew K., and Smith H.S. Correlation of bromodeoxyuridine (BRDU) labeling of breast carcinoma cells with mitotic figure content and tumor grade. Am. J. Surg. Pathol. 17 (1993) 987-994
27. McGinley J.N., Knott K.K., and Thompson H.J. Effect of fixation and epitope retrieval on BrdU indices in mammary carcinomas. J. Histochem. Cytochem. 48 (2000) 355-362
28. Carroll R.E., Matkowskyj K.A., Chakrabarti S., McDonald T.J., and Benya R.V. Aberrant expression of gastrin-releasing peptide and its receptor by well-differentiated colon cancers in humans. Am. J. Physiol. 276 (1999) G655-G665
29. Taneja N., Coy P.E., Lee I., Bryson J.M., and Robey R.B. Proinflammatory interleukin-1 cytokines increase mesangial cell hexokinase activity and hexokinase II isoform abundance. Am. J. Physiol. Cell Physiol. 287 (2004) C548-C557
30. Nogami H., Watanabe T., and Kobayashi S. IGF-I and IGF-binding protein gene expressions in spontaneous dwarf rat. Am. J. Physiol. 267 (1994) E396-E401
31. Tei T.M., Kissmeyer-Nielsen P., Christensen H., and Flyvbjerg A. Growth hormone treatment increases transmural colonic growth in GH-deficient dwarf rats. Growth Horm. IGF Res. 10 (2000) 85-92
32. Papanikolaou A., Wang Q.S., Delker D.A., and Rosenberg D.W. Azoxymethane-induced colon tumors and aberrant crypt foci in mice of different genetic susceptibility. Cancer Lett. 130 (1998) 29-34
33. Papanikolaou A., Wang Q., Delker D.A., and Rosenberg D.W. Azoxymethane-induced colon tumors and aberrant crypt foci in mice of different genetic susceptibility. Cancer Lett. 130 (1998) 29-34
34. Cameron I.L., Garza J., and Hardman W.E. Distribution of lymphoid nodules, aberrant crypt foci and tumours in the colon of carcinogen-treated rats. Br. J. Cancer 73 (1996) 893-898
35. Deschner E.E., and Maskens A.P. Significance of the labeling index and labeling distribution as kinetic parameters in colorectal mucosa of cancer patients and DMH treated animals. Cancer 50 (1982) 1136-1141
36. Robey R.B., and Hay N. Mitochondrial hexokinases: guardians of the mitochondria. Cell Cycle 4 (2005) 654-658
37. van Diest P.J., Brugal G., and Baak J.P. Proliferation markers in tumours: interpretation and clinical value. J. Clin. Pathol. 51 (1998) 716-724
38. Pollak M. Insulin and insulin-like growth factor signalling in neoplasia. Nat. Rev. Cancer 8 (2008) 915-928
39. Charlton H.M., Clark R.G., Robinson I.C., Goff A.E., Cox B.S., Bugnon C., and Bloch B.A. Growth hormone-deficient dwarfism in the rat: a new mutation. J. Endocrinol. 119 (1988) 51-58
40. Ealey K.N., Xuan W., Lu S., and Archer M.C. Colon carcinogenesis in liver-specific IGF-I-deficient (LID) mice. Int. J. Cancer 122 (2008) 472-476
41. Volate S.R., Davenport D.M., Muga S.J., and Wargovich M.J. Modulation of aberrant crypt foci and apoptosis by dietary herbal supplements (quercetin, curcumin, silymarin, ginseng and rutin). Carcinogenesis 26 (2005) 1450-1456
42. Reddy B.S. Prevention of colon cancer by pre- and probiotics: evidence from laboratory studies. Br. J. Nutr. 80 (1998) S219-S223
43. Papanikolaou A., Shank R.C., Delker D.A., Povey A., Cooper D.P., and Rosenberg D.W. Initial levels of azoxymethane-induced DNA methyl adducts are not predictive of tumor susceptibility in inbred mice. Toxicol. Appl. Pharmacol. 150 (1998) 196-203
44. Jackson P.E., O'Connor P.J., Cooper D.P., Margison G.P., and Povey A.C. Associations between tissue-specific DNA alkylation, DNA repair and cell proliferation in the colon and colon tumour yield in mice treated with 1, 2-dimethylhydrazine. Carcinogenesis 24 (2003) 527-533
45. Swanson S.M., and Unterman T.G. The growth hormone-deficient Spontaneous Dwarf rat is resistant to chemically induced mammary carcinogenesis. Carcinogenesis 23 (2002) 977-982
46. Kupper J.H., Muller M., and Wolf I. NAD(+) consumption in carcinogen-treated hamster cells overexpressing a dominant negative mutant of poly(ADP-ribose) polymerase. Biochem. Biophys. Res. Commun. 265 (1999) 525-529
47. Nordling M.M., Nygren J., Bergman J., Sundberg K., and Rafter J.J. Toxicological characterization of a novel in vivo benzo[a]pyrene metabolite, 7-oxo-benz[d]anthracene-3,4-dicarboxylic acid anhydride. Chem. Res. Toxicol. 15 (2002) 1274-1280
48. Poole A.J., Heap D., Carroll R.E., and Tyner A.L. Tumor suppressor functions for the Cdk inhibitor p21 in the mouse colon. Oncogene 23 (2004) 8128-8134
49. Ngo T.H., Barnard R.J., Leung P.S., Cohen P., and Aronson W.J. Insulin-like growth factor I (IGF-I) and IGF binding protein-1 modulate prostate cancer cell growth and apoptosis: possible mediators for the effects of diet and exercise on cancer cell survival. Endocrinology 144 (2003) 2319-2324
50. Hurbin A., Coll J.L., Dubrez-Daloz L., Mari B., Auberger P., Brambilla C., and Favrot M.C. Cooperation of amphiregulin and insulin-like growth factor-1 inhibits Bax- and Bad-mediated apoptosis via a protein kinase C-dependent pathway in non-small cell lung cancer cells. J. Biol. Chem. 280 (2005) 19757-19767
51. Costoya J.A., Finidori J., Moutoussamy S., Searis R., Devesa J., and Arce V.M. Activation of growth hormone receptor delivers an antiapoptotic signal: evidence for a role of Akt in this pathway. Endocrinology 140 (1999) 5937-5943
52. Yamauchi T., Ueki K., Tobe K., Tamemoto H., Sekine N., Wada M., Honjo M., Takahashi M., Takahashi T., Hirai H., Tsushima T., Akanuma Y., Fujita T., Komuro I., Yazaki Y., and Kadowaki T. Growth hormone-induced tyrosine phosphorylation of EGF receptor as an essential element leading to MAP kinase activation and gene expression. Endocr. J. 45 Suppl. (1998) S27-S31
53. Eshet R., Werner H., Klinger B., Silbergeld A., Laron Z., LeRoith D., and Roberts Jr. C.T. Up-regulation of insulin-like growth factor-I (IGF-I) receptor gene expression in patients with reduced serum IGF-I levels. J. Mol. Endocrinol. 10 (1993) 115-120
54. Ewton D.Z., Kansra S., Lim S., and Friedman E. Insulin-like growth factor-I has a biphasic effect on colon carcinoma cells through transient inactivation of forkhead1, initially mitogenic, then mediating growth arrest and differentiation. Int. J. Cancer 98 (2002) 665-673
55. Yang W., Bancroft L., Nicholas C., Lozonschi I., and Augenlicht L.H. Targeted inactivation of p27kip1 is sufficient for large and small intestinal tumorigenesis in the mouse, which can be augmented by a Western-style high-risk diet. Cancer Res. 63 (2003) 4990-4996
56. Hagos G.K., Carroll R.E., Kouznetsova T., Li Q., Toader V., Fernandez P.A., Swanson S.M., and Thatcher G.R. Colon cancer chemoprevention by a novel NO chimera that shows anti-inflammatory and antiproliferative activity in vitro and in vivo. Mol. Cancer Ther. 6 (2007) 2230-2239
57. Besson A. p27Kip1: tumor suppressor and oncogene?. Med. Sci. (Paris) 23 (2007) 1089-1091
58. Corpet D.E., and Tache S. Most effective colon cancer chemopreventive agents in rats: a systematic review of aberrant crypt foci and tumor data, ranked by potency. Nutr. Cancer 43 (2002) 1-21
59. Pollak M., Blouin M.J., Zhang J.C., and Kopchick J.J. Reduced mammary gland carcinogenesis in transgenic mice expressing a growth hormone antagonist. Br. J. Cancer 85 (2001) 428-430
60. Anzo M., Cobb L.J., Hwang D.L., Mehta H., Said J.W., Yakar S., LeRoith D., and Cohen P. Targeted deletion of hepatic Igf1 in TRAMP mice leads to dramatic alterations in the circulating insulin-like growth factor axis but does not reduce tumor progression. Cancer Res. 68 (2008) 3342-3349
61. Yamada Y., Yoshimi N., Hirose Y., Kawabata K., Matsunaga K., Shimizu M., Hara A., and Mori H. Frequent beta-catenin gene mutations and accumulations of the protein in the putative preneoplastic lesions lacking macroscopic aberrant crypt foci appearance, in rat colon carcinogenesis. Cancer Res. 60 (2000) 3323-3327
62. Femia A.P., Dolara P., and Caderni G. Mucin-depleted foci (MDF) in the colon of rats treated with azoxymethane (AOM) are useful biomarkers for colon carcinogenesis. Carcinogenesis 25 (2004) 277-281
63. Schmelz E.M., Levi E., Du J., Xu H., and Majumdar A.P. Age-related loss of EGF-receptor related protein (ERRP) in the aging colon is a potential risk factor for colon cancer. Mech. Ageing Dev. 125 (2004) 917-922
64. Martinoli M.G., Ouellet J., Rheaume E., and Pelletier G. Growth hormone and somatostatin gene expression in adult and aging rats as measured by quantitative in situ hybridization. Neuroendocrinology 54 (1991) 607-615
65. Velasco B., Cacicedo L., Melian E., Fernandez-Vazquez G., and Sanchez-Franco F. Sensitivity to exogenous GH and reversibility of the reduced IGF-I gene expression in aging rats. Eur. J. Endocrinol. 145 (2001) 73-85
66. Michaylira C.Z., Simmons J.G., Ramocki N.M., Scull B.P., McNaughton K.K., Fuller C.R., and Lund P.K. Suppressor of cytokine signaling-2 limits intestinal growth and enterotrophic actions of IGF-I in vivo. Am. J. Physiol. Gastrointest. Liver Physiol. 291 (2006) G472-G481
67. Klurfeld D.M., Weber M.M., and Kritchevsky D. Inhibition of chemically induced mammary and colon tumor promotion by caloric restriction in rats fed increased dietary fat. Cancer Res. 47 (1987) 2759-2762
68. Dunn S.E., Kari F.W., French J., Leininger J.R., Travlos G., Wilson R., and Barrett J.C. Dietary restriction reduces insulin-like growth factor I levels, which modulates apoptosis, cell proliferation, and tumor progression in p53-deficient mice. Cancer Res. 57 (1997) 4667-4672
69. Stewart J.W., Koehler K., Jackson W., Hawley J., Wang W., Au A., Myers R., and Birt D.F. Prevention of mouse skin tumor promotion by dietary energy restriction requires an intact adrenal gland and glucocorticoid supplementation restores inhibition. Carcinogenesis 26 (2005) 1077-1084
70. Moore T., Carbajal S., Beltran L., Perkins S.N., Yakar S., Leroith D., Hursting S.D., and Digiovanni J. Reduced susceptibility to two-stage skin carcinogenesis in mice with low circulating insulin-like growth factor I levels. Cancer Res. 68 (2008) 3680-3688
71. Raguso C.A., Leverve X., and Pichard C. Protective effects of recombinant growth hormone on intestinal mucosa in rats receiving abdominal radiotherapy. Clin. Nutr. 21 (2002) 487-490
72. Williams K.L., Fuller C.R., Dieleman L.A., DaCosta C.M., Haldeman K.M., Sartor R.B., and Lund P.K. Enhanced survival and mucosal repair after dextran sodium sulfate-induced colitis in transgenic mice that overexpress growth hormone. Gastroenterology 120 (2001) 925-937