Human xeno-autoantibodies against a non-human sialic acid serve as novel serum biomarkers and immunotherapeutics in cancer

Cancer Research

Volumn 71, Issue 9, 2011, Pages 3352-3363

  Padler Karavani, Vered ^a   Hurtado Ziola, Nancy ^c   Pu, Minya ^a   Yu, Hai ^d   Huang, Shengshu ^d   Muthana, Saddam ^d   Chokhawala, Harshal A ^d   Cao, Hongzhi ^d   Secrest, Patrick ^a   Friedmann Morvinski, Dinorah ^b   Singer, Oded ^b   Ghaderi, Darius ^c   Verma, Inder M ^b   Liu, Yu Tsueng ^a   Messer, Karen ^a   Chen, Xi ^d   Varki, Ajit ^a   Schwab, Richard ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c Sialix Inc   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; BIOLOGICAL MARKER; EPITOPE; IMMUNOGLOBULIN G; N ACETYLNEURAMINIC ACID; N GLYCOLOYLNEURAMINIC ACID; N GLYCOLOYLNEURAMINIC ACID ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY BLOOD LEVEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; BREAST CANCER; CELL KILLING; COLON ADENOCARCINOMA; COLON CANCER; COMPLEMENT SYSTEM; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DISEASE MARKER; ENDOMETRIUM CANCER; FEMALE; HUMAN; HUMAN CELL; LUNG CANCER; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY CANCER; PANCREAS CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN PURIFICATION; SERUM;

ADENOCARCINOMA; ANIMALS; AUTOANTIBODIES; BREAST NEOPLASMS; COLONIC NEOPLASMS; HUMANS; IMMUNIZATION, PASSIVE; IMMUNOGLOBULIN G; IMMUNOGLOBULINS, INTRAVENOUS; JURKAT CELLS; MICE; MICE, INBRED C57BL; N-ACETYLNEURAMINIC ACID; NEOPLASMS; TUMOR MARKERS, BIOLOGICAL;

EID: 79955488798     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-4102     Document Type: Article

References (48)

1. Varki A, Kannagi R, Toole BP. Glycosylation changes in cancer. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME, editors. Essentials of Glycobiology. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2009. p. 617-32.
2. Malykh YN, Schauer R, Shaw L. N-Glycolylneuraminic acid in human tumours. Biochimie 2001;83:623-34. (Pubitemid 32821226)
3. Tangvoranuntakul P, Gagneux P, Diaz S, Bardor M, Varki N, Varki A, et al. Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc Natl Acad Sci U S A 2003;100:12045-50. (Pubitemid 37271512)
4. Nguyen DH, Tangvoranuntakul P, Varki A. Effects of natural human antibodies against a nonhuman sialic acid that metabolically incorporates into activated and malignant immune cells. J Immunol 2005;175:228-36. (Pubitemid 40884323)
5. Padler-Karavani V, Yu H, Cao H, Chokhawala H, Karp F, Varki N, et al. Diversity in specificity, abundance, and composition of anti-Neu5Gc antibodies in normal humans: potential implications for disease. Glycobiology 2008;18:818-30.
6. Varki A. Colloquium paper: uniquely human evolution of sialic acid genetics and biology. Proc Natl Acad Sci U S A 2010;107 Suppl 2:8939-46.
7. Hedlund M, Tangvoranuntakul P, Takematsu H, Long JM, Housley GD, Kozutsumi Y, et al. N-glycolylneuraminic acid deficiency in mice: implications for human biology and evolution. Mol Cell Biol 2007; 27:4340-6. (Pubitemid 46906558)
8. Taylor RE, Gregg CJ, Padler-Karavani V, Ghaderi D, Yu H, Huang S, et al. Novel mechanism for the generation of human xeno-autoantibodies against the nonhuman sialic acid N-glycolylneuraminic acid. J Exp Med 2010;207:1637-46.
9. Hedlund M, Padler-Karavani V, Varki NM, Varki A. Evidence for a human-specific mechanism for diet and antibody-mediated inflammation in carcinoma progression. Proc Natl Acad Sci U S A 2008;105:18936-41.
10. de Visser KE, Korets LV, Coussens LM. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 2005;7:411-23. (Pubitemid 40719125)
11. Andreu P, Johansson M, Affara NI, Pucci F, Tan T, Junankar S, et al. FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 2010;17:121-34.
12. Adams GP, Weiner LM. Monoclonal antibody therapy of cancer. Nat Biotechnol 2005;23:1147-57. (Pubitemid 41486396)
13. Ferris RL, Jaffee EM, Ferrone S. Tumor antigen-targeted, monoclonal antibody-based immunotherapy: clinical response, cellular immunity, and immunoescape. J Clin Oncol 2010;28:4390-9.
14. Finn OJ. Cancer immunology. N Engl J Med 2008;358:2704-15.
15. Prehn RT, Prehn LM. The flip side of immune surveillance: immune dependency. Immunol Rev 2008;222:341-56. (Pubitemid 351430371)
16. Marcial VA. Carcinoma of the cervix: present status and future. Cancer 1977;39:945-58. (Pubitemid 8060288)
17. Nelson HD, Tyne K, Naik A, Bougatsos C, Chan BK, Humphrey L. Screening for breast cancer: an update for the U.S. Preventive Services Task Force. Ann Intern Med 2009;151:727-37, W237-42.
18. Ludwig JA, Weinstein JN. Biomarkers in cancer staging, prognosis and treatment selection. Nat Rev Cancer 2005;5:845-56. (Pubitemid 41746029)
19. Gupta D, Lis CG. Role of CA125 in predicting ovarian cancer survival - a review of the epidemiological literature. J Ovarian Res 2009;2:13.
20. Schröder FH, Hugosson J, Roobol MJ, Tammela TL, Ciatto S, Nelen V, et al. Screening and prostate-cancer mortality in a randomized European study. N Engl J Med 2009;360:1320-8.
21. Tan HT, Low J, Lim SG, Chung MC. Serum autoantibodies as biomarkers for early cancer detection. FEBS J 2009;276:6880-904.
22. Soussi T. p53Antibodies in the sera of patients with various types of cancer: a review. Cancer Res 2000;60:1777-88.
23. Drake PM, Cho W, Li B, Prakobphol A, Johansen E, Anderson NL, et al. Sweetening the pot: adding glycosylation to the biomarker discovery equation. Clin Chem 2010;56:223-36.
24. Singer O, Marr RA, Rockenstein E, Crews L, Coufal NG, Gage FH, et al. Targeting BACE1 with siRNAs ameliorates Alzheimer disease neuropathology in a transgenic model. Nat Neurosci 2005;8: 1343-9. (Pubitemid 41630422)
25. Tiscornia G, Singer O, Verma IM. Production and purification of lentiviral vectors. Nat Protoc 2006;1:241-5.
26. Bardor M, Nguyen DH, Diaz S, Varki A. Mechanism of uptake and incorporation of the non-human sialic acid N-glycolylneuraminic acid into human cells. J Biol Chem 2005;280:4228-37. (Pubitemid 40288589)
27. Yu H, Chokhawala HA, Huang S, Chen X. One-pot three-enzyme chemoenzymatic approach to the synthesis of sialosides containing natural and non-natural functionalities. Nat Protoc 2006;1: 2485-92.
28. Yu H, Huang S, Chokhawala H, Sun M, Zheng H, Chen X. Highly efficient chemoenzymatic synthesis of naturally occurring and nonnatural alpha-2,6-linked sialosides: a P. damsela alpha-2,6-sialyltransferase with extremely flexible donor-substrate specificity. Angew Chem Int Ed Engl 2006;45:3938-44. (Pubitemid 44105691)
29. Yu H, Chokhawala H, Karpel R, Yu H, Wu B, Zhang J, et al. A multifunctional Pasteurella multocida sialyltransferase: a powerful tool for the synthesis of sialoside libraries. J Am Chem Soc 2005;127: 17618-9. (Pubitemid 43003372)
30. Jolles S, Sewell WA, Misbah SA. Clinical uses of intravenous immunoglobulin. Clin Exp Immunol 2005;142:1-11. (Pubitemid 41360999)
31. Oyelaran O, McShane LM, Dodd L, Gildersleeve JC. Profiling human serum antibodies with a carbohydrate antigen microarray. J Proteome Res 2009;8:4301-10.
32. Datta A, Bansal V, Diaz J, Patel J, Reato D, Bikson M, et al. Sensitive and specific detection of the non-human sialic Acid N-glycolylneuraminic acid in human tissues and biotherapeutic products. PLoS ONE 2009;4:e4241.
33. Thompson IM, Ankerst DP, Chi C, Lucia MS, Goodman PJ, Crowley JJ, et al. Operating characteristics of prostate-specific antigen in men with an initial PSA level of 3.0 ng/ml or lower. JAMA 2005;294:66-70. (Pubitemid 41002840)
34. Cavadas V, Osorio L, Sabell F, Teves F, Branco F, Silva-Ramos M. Prostate cancer prevention trial and European randomized study of screening for prostate cancer risk calculators: a performance comparison in a contemporary screened cohort. Eur Urol 2010;58:551-8.
35. Martin LT, Marth JD, Varki A, Varki NM. Genetically altered mice with different sialyltransferase deficiencies show tissue-specific alterations in sialylation and sialic acid 9-O-acetylation. J Biol Chem 2002;277: 32930-8. (Pubitemid 34987555)
36. Conze T, Carvalho AS, Landegren U, Almeida R, Reis CA, David L, et al. MUC2 mucin is a major carrier of the cancer-associated sialyl-Tn antigen in intestinal metaplasia and gastric carcinomas. Glycobiology 2010;20:199-206.
37. Yonezawa S, Tachikawa T, Shin S, Sato E. Sialosyl-Tn antigen. Its distribution in normal human tissues and expression in adenocarcinomas. Am J Clin Pathol 1992;98:167-74.
38. Cao Y, Stosiek P, Springer GF, Karsten U. Thomsen-Friedenreichrelated carbohydrate antigens in normal adult human tissues: a systematic and comparative study. Histochem Cell Biol 1996;106: 197-207.
39. Ogata S, Koganty R, Reddish M, Longenecker BM, Chen A, Perez C, et al. Different modes of sialyl-Tn expression during malignant transformation of human colonic mucosa. Glycoconj J 1998;15:29-35. (Pubitemid 28085543)
40. Kobayashi H, Terao T, Kawashima Y. Serum sialyl Tn as an independent predictor of poor prognosis in patients with epithelial ovarian cancer. J Clin Oncol 1992;10:95-101.
41. Imai J, Ghazizadeh M, Naito Z, Asano G. Immunohistochemical expression of T, Tn and sialyl-Tn antigens and clinical outcome in human breast carcinoma. Anticancer Res 2001;21:1327-34.
42. Kim GE, Bae HI, Park HU, Kuan SF, Crawley SC, Ho JJ, et al. Aberrant expression of MUC5AC and MUC6 gastric mucins and sialyl Tn antigen in intraepithelial neoplasms of the pancreas. Gastroenterology 2002;123:1052-60.
43. Ju T, Cummings RD.A unique molecular chaperone Cosmc required for activity of the mammalian core 1 beta 3-galactosyltransferase. Proc Natl Acad Sci U S A 2002;99:16613-8. (Pubitemid 36034021)
44. Ju T, Lanneau GS, Gautam T, Wang Y, Xia B, Stowell SR, et al. Human tumor antigens Tn and sialyl Tn arise from mutations in Cosmc. Cancer Res 2008;68:1636-46. (Pubitemid 351416547)
45. Sewell R, Bäckström M, Dalziel M, Gschmeissner S, Karlsson H, Noll T, et al. The ST6GalNAc-I sialyltransferase localizes throughout the Golgi and Is responsible for the synthesis of the tumor-associated sialyl-Tn O-glycan in human breast cancer. J Biol Chem 2006;281: 3586-94. (Pubitemid 43845976)
46. Ostrand-Rosenberg S.Immune surveillance: a balance between protumor and antitumor immunity. Curr Opin Genet Dev 2008;18: 11-8.
47. Slovin SF, Keding SJ, Ragupathi G. Carbohydrate vaccines as immunotherapy for cancer. Immunol Cell Biol 2005;83:418-28. (Pubitemid 41044620)
48. + regulatory T cells function. Int Immunol 2008;20:591-600.