Insulin resistance in vascular endothelial cells promotes intestinal tumour formation

Oncogene

Volumn 36, Issue 35, 2017, Pages 4987-4996

  Wang, X ^a,b   Haring M F ^a,c   Rathjen, T ^a,d   Lockhart, S M ^a,e   Sorensen D ^a,f,g   Ussar, S ^a,h,i   Rasmussen, L M ^f   Bertagnolli, M M ^j   Kahn, C R ^a   Rask Madsen, C ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b FUDAN UNIVERSITY   (China)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d NOVO NORDISK A S   (Denmark)

^e QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^f ODENSE UNIVERSITY HOSPITAL   (Denmark)

^g The Danish Diabetes Academy   (Denmark)

^h INSTITUTE OF EPIDEMIOLOGY   (Germany)

ⁱ GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^j BRIGHAM AND WOMEN S HOSPITAL   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; INSULIN RECEPTOR; TUMOR NECROSIS FACTOR; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER RISK; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; HYPERINSULINEMIA; IN VITRO STUDY; INSULIN RESISTANCE; INSULIN SIGNALING; INTESTINE EPITHELIUM CELL; INTESTINE TUMOR; LEUKOCYTE ADHERENCE; LIPID DIET; LOW FAT DIET; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIMARY CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH CARCINOGENESIS; TUMOR CELL; TUMOR CELL CULTURE; TUMOR MICROENVIRONMENT; VASCULAR ENDOTHELIAL CELL; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CARCINOGENESIS; COLORECTAL TUMOR; ENDOTHELIUM CELL; GENE SILENCING; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CARCINOGENESIS; COLORECTAL NEOPLASMS; ENDOTHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; INSULIN; INSULIN RESISTANCE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; VASCULAR CELL ADHESION MOLECULE-1;

EID: 85028665915     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2017.107     Document Type: Article

References (58)

1. Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet 2008; 371: 569-578.
2. Yuhara H, Steinmaus C, Cohen SE, Corley DA, Tei Y, Buffler PA. Is diabetes mellitus an independent risk factor for colon cancer and rectal cancer? Am J Gastroenterol 2011; 106: 1911-1921.
3. Gallagher EJ, LeRoith D. Obesity and diabetes: the increased risk of cancer and cancer-related mortality. Physiol Rev 2015; 95: 727-748.
4. Pollak M. The insulin and insulin-like growth factor receptor family in neoplasia: an update. Nat Rev Cancer 2012; 12: 159-169.
5. Sandhu MS, Dunger DB, Giovannucci EL. Insulin, insulin-like growth factor-I (IGF-I), IGF binding proteins, their biologic interactions, and colorectal cancer. J Natl Cancer Inst 2002; 94: 972-980.
6. Yoon YS, Keum N, Zhang X, Cho E, Giovannucci EL. Hyperinsulinemia, insulin resistance and colorectal adenomas: a meta-analysis. Metabolism 2015; 64: 1324-1333.
7. Osborne CK, Bolan G, Monaco ME, Lippman ME. Hormone responsive human breast cancer in long-term tissue culture: effect of insulin. Proc Natl Acad Sci USA 1976; 73: 4536-4540.
8. Ish-Shalom D, Christoffersen CT, Vorwerk P, Sacerdoti-Sierra N, Shymko RM, Naor D et al. Mitogenic properties of insulin and insulin analogues mediated by the insulin receptor. Diabetologia 1997; 40(Suppl 2): S25-S31.
9. Kurtzhals P, Schaffer L, Sorensen A, Kristensen C, Jonassen I, Schmid C et al. Correlations of receptor binding and metabolic and mitogenic potencies of insulin analogs designed for clinical use. Diabetes 2000; 49: 999-1005.
10. Giovannucci E. Insulin and colon cancer. Cancer Causes Control: CCC 1995; 6: 164-179.
11. Bruce WR, Wolever TM, Giacca A. Mechanisms linking diet and colorectal cancer: the possible role of insulin resistance. Nutr Cancer 2000; 37: 19-26.
12. Khandekar MJ, Cohen P, Spiegelman BM. Molecular mechanisms of cancer development in obesity. Nat Rev Cancer 2011; 11: 886-895.
13. Luck H, Tsai S, Chung J, Clemente-Casares X, Ghazarian M, Revelo XS et al. Regulation of obesity-related insulin resistance with gut anti-inflammatory agents. Cell Metab 2015; 21: 527-542.
14. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 2010; 140: 883-899.
15. Carothers AM, Moran AE, Cho NL, Redston M, Bertagnolli MM. Changes in antitumor response in C57BL/6 J-Min/+ mice during long-term administration of a selective cyclooxygenase-2 inhibitor. Cancer Res 2006; 66: 6432-6438.
16. Bertagnolli MM, Eagle CJ, Zauber AG, Redston M, Solomon SD, Kim K et al. Celecoxib for the prevention of sporadic colorectal adenomas. N Engl J Med 2006; 355: 873-884.
17. Chan AT, Arber N, Burn J, Chia WK, Elwood P, Hull MA et al. Aspirin in the chemoprevention of colorectal neoplasia: an overview. Cancer Prev Res (Phila) 2012; 5: 164-178.
18. Rask-Madsen C, Li Q, Freund B, Feather D, Abramov R, Wu IH et al. Loss of insulin signaling in vascular endothelial cells accelerates atherosclerosis in apolipoprotein E null mice. Cell Metab 2010; 11: 379-389.
19. Kim F, Pham M, Maloney E, Rizzo NO, Morton GJ, Wisse BE et al. Vascular inflammation, insulin resistance, and reduced nitric oxide production precede the onset of peripheral insulin resistance. Arterioscler Thromb Vasc Biol 2008; 28: 1982-1988.
20. Zhao L, Fu Z, Wu J, Aylor KW, Barrett EJ, Cao W et al. Inflammation-induced microvascular insulin resistance is an early event in diet-induced obesity. Clin Sci (Lond) 2015; 129: 1025-1036.
21. Laakso M, Edelman SV, Brechtel G, Baron AD. Impaired insulin-mediated skeletal muscle blood flow in patients with NIDDM. Diabetes 1992; 41: 1076-1083.
22. Steinberg HO, Chaker H, Leaming R, Johnson A, Brechtel G, Baron AD. Obesity/ insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance. J Clin Invest 1996; 97: 2601-2610.
23. Rask-Madsen C, Ihlemann N, Krarup T, Christiansen E, Kober L, Nervil Kistorp C et al. Insulin therapy improves insulin-stimulated endothelial function in patients with type 2 diabetes and ischemic heart disease. Diabetes 2001; 50: 2611-2618.
24. Tabit CE, Shenouda SM, Holbrook M, Fetterman JL, Kiani S, Frame AA et al. Protein kinase C-beta contributes to impaired endothelial insulin signaling in humans with diabetes mellitus. Circulation 2013; 127: 86-95.
25. Alva JA, Zovein AC, Monvoisin A, Murphy T, Salazar A, Harvey NL et al. VE-Cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells. Dev Dyn 2006; 235: 759-767.
26. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007; 45: 593-605.
27. Vicent D, Ilany J, Kondo T, Naruse K, Fisher SJ, Kisanuki YY et al. The role of endothelial insulin signaling in the regulation of vascular tone and insulin resistance. J Clin Invest 2003; 111: 1373-1380.
28. Gey GT, Thalhimer W. Observations on the effects of insulin introduced into the medium of tissue cultures. JAMA 1924; 82: 1609.
29. Temin HM. Carcinogenesis by avian sarcoma viruses. X. The decreased requirement for insulin-replaceable activity in serum for cell multiplication. Int J Cancer 1968; 3: 771-787.
30. Raizada MK, Perdue JF. Mitogen receptors in chick embryo fibroblasts. Kinetics, specificity, unmasking, and synthesis of 125I-insulin binding sites. J Biol Chem 1976; 251: 6445-6455.
31. Koenuma M, Yamori T, Tsuruo T. Insulin and insulin-like growth factor 1 stimulate proliferation of metastatic variants of colon carcinoma 26. Jpn J Cancer Res 1989; 80: 51-58.
32. Makinen J, Hannukainen JC, Karmi A, Immonen HM, Soinio M, Nelimarkka L et al. Obesity-associated intestinal insulin resistance is ameliorated after bariatric surgery. Diabetologia 2015; 58: 1055-1062.
33. Monteiro-Sepulveda M, Touch S, Mendes-Sa C, Andre S, Poitou C, Allatif O et al. Jejunal T cell inflammation in human obesity correlates with decreased enterocyte insulin signaling. Cell Metab 2015; 22: 113-124.
34. Novosyadlyy R, Lann DE, Vijayakumar A, Rowzee A, Lazzarino DA, Fierz Y et al. Insulin-mediated acceleration of breast cancer development and progression in a nonobese model of type 2 diabetes. Cancer Res 2010; 70: 741-751.
35. Rostoker R, Abelson S, Bitton-Worms K, Genkin I, Ben-Shmuel S, Dakwar M et al. Highly specific role of the insulin receptor in breast cancer progression. Endocr Relat Cancer 2015; 22: 145-157.
36. Treffers LW, Hiemstra IH, Kuijpers TW, van den Berg TK, Matlung HL. Neutrophils in cancer. Immunol Rev 2016; 273: 312-328.
37. Coffelt SB, Wellenstein MD, de Visser KE. Neutrophils in cancer: neutral no more. Nat Rev Cancer 2016; 16: 431-446.
38. Jamieson T, Clarke M, Steele CW, Samuel MS, Neumann J, Jung A et al. Inhibition of CXCR2 profoundly suppresses inflammation-driven and spontaneous tumorigenesis. J Clin Invest 2012; 122: 3127-3144.
39. Ellis LM, Hicklin DJ. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat Rev Cancer 2008; 8: 579-591.
40. Fukumura D, Salehi HA, Witwer B, Tuma RF, Melder RJ, Jain RK. Tumor necrosis factor alpha-induced leukocyte adhesion in normal and tumor vessels: effect of tumor type, transplantation site, and host strain. Cancer Res 1995; 55: 4824-4829.
41. Melder RJ, Koenig GC, Witwer BP, Safabakhsh N, Munn LL, Jain RK. During angiogenesis, vascular endothelial growth factor and basic fibroblast growth factor regulate natural killer cell adhesion to tumor endothelium. Nat Med 1996; 2: 992-997.
42. Steyers CM 3rd, Miller FJ Jr. Endothelial dysfunction in chronic inflammatory diseases. Int J Mol Sci 2014; 15: 11324-11349.
43. Bickston SJ, Behm BW, Tsoulis DJ, Cheng J, MacDonald JK, Khanna R et al. Vedolizumab for induction and maintenance of remission in ulcerative colitis. Cochrane Database Syst Rev 2014; 8: CD007571.
44. Fischer A, Zundler S, Atreya R, Rath T, Voskens C, Hirschmann S et al. Differential effects of alpha4beta7 and GPR15 on homing of effector and regulatory T cells from patients with UC to the inflamed gut in vivo. Gut 2015; 65: 1642-1664.
45. Targan SR, Feagan BG, Fedorak RN, Lashner BA, Panaccione R, Present DH et al. Natalizumab for the treatment of active Crohn's disease: results of the ENCORE Trial. Gastroenterology 2007; 132: 1672-1683.
46. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009; 457: 608-611.
47. Dow LE, O'Rourke KP, Simon J, Tschaharganeh DF, van Es JH, Clevers H et al. Apc restoration promotes cellular differentiation and reestablishes crypt homeostasis in colorectal cancer. Cell 2015; 161: 1539-1552.
48. Elmunzer BJ, Hayward RA, Schoenfeld PS, Saini SD, Deshpande A, Waljee AK. Effect of flexible sigmoidoscopy-based screening on incidence and mortality of colorectal cancer: a systematic review and meta-analysis of randomized controlled trials. PLoS Med 2012; 9: e1001352.
49. Okabayashi K, Ashrafian H, Hasegawa H, Yoo JH, Patel VM, Harling L et al. Body mass index category as a risk factor for colorectal adenomas: a systematic review and meta-analysis. Am J Gastroenterol 2012; 107: 1175-1185, quiz 86.
50. Davenport JR, Su T, Zhao Z, Coleman HG, Smalley WE, Ness RM et al. Modifiable lifestyle factors associated with risk of sessile serrated polyps, conventional adenomas and hyperplastic polyps. Gut; epub ahead of print 15 November 2016; doi:10. 1136/gutjnl-2016-312893.
51. Anderson JC, Weiss JE, Robinson CM, Butterly LF. Adenoma detection rates for screening colonoscopies in smokers and obese adults: data from the New Hampshire colonoscopy registry. J Clin Gastroenterol; epub ahead of print 5 January 2017; doi:10. 1136/gutjnl-2016-312893.
52. Flores MB, Rocha GZ, Damas-Souza DM, Osorio-Costa F, Dias MM, Ropelle ER et al. Obesity-induced increase in tumor necrosis factor-alpha leads to development of colon cancer in mice. Gastroenterology 2012; 143: 741-753 e1-4.
53. Naruse K, Rask-Madsen C, Takahara N, Ha SW, Suzuma K, Way KJ et al. Activation of vascular protein kinase C-beta inhibits Akt-dependent endothelial nitric oxide synthase function in obesity-associated insulin resistance. Diabetes 2006; 55: 691-698.
54. Jiang ZY, Lin YW, Clemont A, Feener EP, Hein KD, Igarashi M et al. Characterization of selective resistance to insulin signaling in the vasculature of obese Zucker (fa/fa) rats. J Clin Invest 1999; 104: 447-457.
55. Rask-Madsen C, Kahn CR. Tissue-specific insulin signaling, metabolic syndrome, and cardiovascular disease. Arterioscler Thromb Vasc Biol 2012; 32: 2052-2059.
56. Michael MD, Kulkarni RN, Postic C, Previs SF, Shulman GI, Magnuson MA et al. Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell 2000; 6: 87-97.
57. Moser AR, Pitot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 1990; 247: 322-324.
58. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem 2002; 277: 33275-33283.