A red meat-derived glycan promotes inflammation and cancer progression

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

Volumn 112, Issue 2, 2015, Pages 542-547

  Samraj, Annie N ^a   Pearce, Oliver M T ^a   Läubli, Heinz ^a   Crittenden, Alyssa N ^a   Bergfeld, Anne K ^a   Band, Kalyan ^a   Gregg, Christopher J ^a   Bingman, Andrea E ^a   Secrest, Patrick ^a   Diaz, Sandra L ^a   Varki, Nissi M ^a   Varki, Ajit ^a,b   Kornfeld, Stuart A ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

N glycolylneuraminic acid; Red meat and cancer; Tumor associated carbohydrate antigen; Tumor associated inflammation; Xenosialitis

Indexed keywords

GLYCAN; N GLYCOLOYLNEURAMINIC ACID; SIALIC ACID; BLOCKING ANTIBODY; CMPACETYLNEURAMINATE MONOOXYGENASE; MIXED FUNCTION OXIDASE; N ACETYLNEURAMINIC ACID; N-GLYCOLYLNEURAMINIC ACID; NEURAMINIC ACID DERIVATIVE;

ACTIVE IMMUNIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER INCIDENCE; CONTROLLED STUDY; FOOD INTAKE; HUMAN; HUMAN TISSUE; INFLAMMATION; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; RED MEAT; ADVERSE EFFECTS; ANALYSIS; ANIMAL; C57BL MOUSE; CONGENIC STRAIN; DEFICIENCY; DISEASE COURSE; FOOD ANALYSIS; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MEAT; METABOLISM; PATHOLOGY; RISK FACTOR;

MAMMALIA; MUS;

ANIMALS; ANTIBODIES, BLOCKING; DISEASE PROGRESSION; FOOD ANALYSIS; HUMANS; INFLAMMATION; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MEAT; MICE; MICE, CONGENIC; MICE, INBRED C57BL; MICE, KNOCKOUT; MIXED FUNCTION OXYGENASES; N-ACETYLNEURAMINIC ACID; NEURAMINIC ACIDS; RISK FACTORS;

EID: 84920895872     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1417508112     Document Type: Article

References (47)

1. Snowdon DA (1988) Animal product consumption and mortality because of all causes combined, coronary heart disease, stroke, diabetes, and cancer in Seventh-day Adventists. Am J Clin Nutr 48(3, Suppl):739-748.
2. Song Y, Manson JE, Buring JE, Liu S (2004) A prospective study of red meat consumption and type 2 diabetes in middle-aged and elderly women: The women's health study. Diabetes Care 27(9):2108-2115.
3. Sinha R, Cross AJ, Graubard BI, Leitzmann MF, Schatzkin A (2009) Meat intake and mortality: A prospective study of over half a million people. Arch Intern Med 169(6): 562-571.
4. Pan A, et al. (2012) Red meat consumption and mortality: Results from 2 prospective cohort studies. Arch Intern Med 172(7):555-563.
5. Glass CK, Olefsky JM (2012) Inflammation and lipid signaling in the etiology of insulin resistance. Cell Metab 15(5):635-645.
6. Rocha VZ, Libby P (2009) Obesity, inflammation, and atherosclerosis. Nat Rev Cardiol 6(6):399-409.
7. Esmaillzadeh A, et al. (2007) Dietary patterns and markers of systemic inflammation among Iranian women. J Nutr 137(4):992-998.
8. Fraser GE (1999) Associations between diet and cancer, ischemic heart disease, and allcause mortality in non-Hispanic white California Seventh-day Adventists. Am J Clin Nutr 70(3, Suppl):532S-538S.
9. Key TJ, et al. (1999) Mortality in vegetarians and nonvegetarians: Detailed findings from a collaborative analysis of 5 prospective studies. Am J Clin Nutr 70(3, Suppl): 516S-524S.
10. Singh PN, Sabaté J, Fraser GE (2003) Does low meat consumption increase life expectancy in humans? Am J Clin Nutr 78(3, Suppl):526S-532S.
11. Wiseman M (2008) The second World Cancer Research Fund/American Institute for Cancer Research expert report. Food, nutrition, physical activity, and the prevention of cancer: A global perspective. Proc Nutr Soc 67(3):253-256.
12. Fearon ER (2011) Molecular genetics of colorectal cancer. Annu Rev Pathol 6:479-507.
13. Cross AJ, et al. (2010) A large prospective study of meat consumption and colorectal cancer risk: An investigation of potential mechanisms underlying this association. Cancer Res 70(6):2406-2414.
14. Sugimura T, Wakabayashi K, Nakagama H, Nagao M (2004) Heterocyclic amines: Mutagens/carcinogens produced during cooking of meat and fish. Cancer Sci 95(4): 290-299.
15. Stavric B (1994) Biological significance of trace levels of mutagenic heterocyclic aromatic amines in human diet: A critical review. Food Chem Toxicol 32(10):977-994.
16. Hedlund M, Padler-Karavani V, Varki NM, Varki A (2008) Evidence for a human-specific mechanism for diet and antibody-mediated inflammation in carcinoma progression. Proc Natl Acad Sci USA 105(48):18936-18941.
17. Padler-Karavani V, et al. (2011) Human xeno-autoantibodies against a non-human sialic acid serve as novel serum biomarkers and immunotherapeutics in cancer. Cancer Res 71(9):3352-3363.
18. Pearce OM, et al. (2014) Inverse hormesis of cancer growth mediated by narrow ranges of tumor-directed antibodies. Proc Natl Acad Sci USA 111(16):5998-6003.
19. Samraj AN, Läubli H, Varki N, Varki A (2014) Involvement of a non-human sialic Acid in human cancer. Front Oncol 4:33.
20. Varki A (2010) Colloquium paper: Uniquely human evolution of sialic acid genetics and biology. Proc Natl Acad Sci USA 107(Suppl 2):8939-8946.
21. Bergfeld AK, Pearce OM, Diaz SL, Pham T, Varki A (2012) Metabolism of vertebrate amino sugars with N-glycolyl groups: Elucidating the intracellular fate of the nonhuman sialic acid N-glycolylneuraminic acid. J Biol Chem 287(34):28865-28881.
22. Banda K, Gregg CJ, Chow R, Varki NM, Varki A (2012) Metabolism of vertebrate amino sugars with N-glycolyl groups: Mechanisms underlying gastrointestinal incorporation of the non-human sialic acid xeno-autoantigen N-glycolylneuraminic acid. J Biol Chem 287(34):28852-28864.
23. Tangvoranuntakul P, et al. (2003) Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc Natl Acad Sci USA 100(21):12045-12050.
24. Hedlund M, et al. (2007) N-glycolylneuraminic acid deficiency in mice: Implications for human biology and evolution. Mol Cell Biol 27(12):4340-4346.
25. Padler-Karavani V, et al. (2008) Diversity in specificity, abundance, and composition of anti-Neu5Gc antibodies in normal humans: Potential implications for disease. Glycobiology 18(10):818-830.
26. Taylor RE, et al. (2010) Novel mechanism for the generation of human xeno-autoantibodies against the nonhuman sialic acid N-glycolylneuraminic acid. J Exp Med 207(8):1637-1646.
27. Spichtig V, Michaud J, Austin S (2010) Determination of sialic acids in milks and milkbased products. Anal Biochem 405(1):28-40.
28. Chen Y, Pan L, Liu N, Troy FA, Wang B (2014) LC-MS/MS quantification of N-acetylneuraminic acid, N-glycolylneuraminic acid and ketodeoxynonulosonic acid levels in the urine and potential relationship with dietary sialic acid intake and disease in 3- to 5-year-old children. Br J Nutr 111(2):332-341.
29. Li H, Fan X (2014) Quantitative analysis of sialic acids in Chinese conventional foods by HPLC-FLD. Open J Prev Med 4:57.
30. Nakamura K, Kuramoto K, Shibasaki K, Shumiya S, Ohtsubo K (1992) [Age-related incidence of spontaneous tumors in SPF C57BL/6 and BDF1 mice]. Jikken Dobutsu 41(3):279-285. Japanese.
31. Hara S, et al. (1989) Determination of mono-O-acetylated N-acetylneuraminic acids in human and rat sera by fluorometric high-performance liquid chromatography. Anal Biochem 179(1):162-166.
32. Inoue S, Inoue Y (2003) Ultrasensitive analysis of sialic acids and oligo/polysialic acids by fluorometric high-performance liquid chromatography. Methods Enzymol 362: 543-560.
33. Schauer R, Srinivasan GV, Coddeville B, Zanetta JP, Guérardel Y (2009) Low incidence of N-glycolylneuraminic acid in birds and reptiles and its absence in the platypus. Carbohydr Res 344(12):1494-1500.
34. Ghaderi D, Taylor RE, Padler-Karavani V, Diaz S, Varki A (2010) Implications of the presence of N-glycolylneuraminic acid in recombinant therapeutic glycoproteins. Nat Biotechnol 28(8):863-867.
35. Jin X, et al. (2006) Paradoxical effects of short- and long-term interleukin-6 exposure on liver injury and repair. Hepatology 43(3):474-484.
36. Naugler WE, et al. (2007) Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 317(5834):121-124.
37. Balkwill F, Charles KA, Mantovani A (2005) Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7(3):211-217.
38. Tan TT, Coussens LM (2007) Humoral immunity, inflammation and cancer. Curr Opin Immunol 19(2):209-216.
39. Wu X, Ragupathi G, Panageas K, Hong F, Livingston PO (2013) Accelerated tumor growth mediated by sublytic levels of antibody-induced complement activation is associated with activation of the PI3K/AKT survival pathway. Clin Cancer Res 19(17): 4728-4739.
40. Andreu P, et al. (2010) FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 17(2):121-134.
41. Mann JR, Backlund MG, DuBois RN (2005) Mechanisms of disease: Inflammatory mediators and cancer prevention. Nat Clin Pract Oncol 2(4):202-210.
42. Rothwell PM, et al. (2011) Effect of daily aspirin on long-term risk of death due to cancer: Analysis of individual patient data from randomised trials. Lancet 377(9759): 31-41.
43. Grivennikov SI, Greten FR, Karin M (2010) Immunity, inflammation, and cancer. Cell 140(6):883-899.
44. Loft S, Poulsen HE (1996) Cancer risk and oxidative DNA damage in man. J Mol Med (Berl) 74(6):297-312.
45. Sliwkowski MX, Mellman I (2013) Antibody therapeutics in cancer. Science 341(6151): 1192-1198.
46. Manzi AE, Diaz S, Varki A (1990) High-pressure liquid chromatography of sialic acids on a pellicular resin anion-exchange column with pulsed amperometric detection: A comparison with six other systems. Anal Biochem 188(1):20-32.
47. Padler-Karavani V, et al. (2013) A simple method for assessment of human anti- Neu5Gc antibodies applied to Kawasaki disease. PLoS ONE 8(3):e58443.