Method for chronological recording of antigen appearance in human head-hair shafts and its use for monitoring glycation products in diabetes

Journal of Immunological Methods

Volumn 320, Issue 1-2, 2007, Pages 1-17

  Nissimov, Joseph ^a   Elchalal, Uriel ^b   Bakala, Hilaire ^c   Brownlee, Michael ^d   Berry, Elliot ^b   Phillip, Moshe ^e   Milner, Yoram ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e SCHNEIDER CHILDREN S MEDICAL CENTER OF ISRAEL   (Israel)

Author keywords

AGEs; Diabetes monitoring; Early diagnosis; EGAs; Hair surrogate tissue analysis; Non invasive immunodetection

Indexed keywords

ADVANCED GLYCATION END PRODUCT; HEMOGLOBIN A1C;

ADULT; ARTICLE; CHEMOLUMINESCENCE; CLINICAL LABORATORY; CONTROLLED STUDY; DENSITOMETRY; DIABETIC PATIENT; DOT HYBRIDIZATION; FEMALE; GLYCATION; GLYCEMIC CONTROL; HAIR; HOSPITALIZATION; HUMAN; IMMUNOASSAY; IMMUNOCHEMISTRY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; PREGNANCY DIABETES MELLITUS; PRIORITY JOURNAL; SCALP HAIR; STATISTICAL SIGNIFICANCE; WESTERN BLOTTING;

ADULT; ANTIGENS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CASE-CONTROL STUDIES; DENSITOMETRY; DIABETES MELLITUS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FEMALE; GLYCOSYLATION; GLYCOSYLATION END PRODUCTS, ADVANCED; HAIR; HUMANS; HYPERGLYCEMIA; IMMUNOBLOTTING; MALE; SCALP;

EID: 33847416668     PISSN: 00221759     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jim.2006.10.014     Document Type: Article

References (95)

1. Ahmed N., Argirov O.K., Minhas H.S., Cordeiro C.A.A., and Thornalley P.J. Assay of advanced glycation endproducts (AGEs): surveying AGEs by chromatographic assay with derivatization by 6-aminoquinoyl-N-hydroxysuccinimidyl-carbamate and application to N-(epsilon)-carboxymethyl-lysine and N-(epsilon-(1-carboxyethyl)-lysine-modified albumin. Biochem. J. 364 (2002) 1
2. Al-Delaimy W.K. Hair as a biomarker for exposure to tobacco smoke. Tob. Control 11 (2002) 176
3. Ando Y., Anan I., Suhr O., Holmgren G., and Costa P.M. Detection of a variant protein in hair: new diagnostic method in Portuguese type familial amyloid polyneuropathy. Br. Med. J. 316 (1998) 1500
4. Araki N., Ueno N., Chakrabarti B., Morino Y., and Horiuchi S. Immunochemical evidence for the presence of advanced glycation end products in human lens proteins and its positive correlation with aging. J. Biol. Chem. 267 (1992) 10211
5. Aronson D., and Rayfield E.J. How hyperglycemia promotes atherosclerosis: molecular mechanisms. Cardiovasc. Diabetol. 1 (2002) 1
6. Barman J.M., Pecoraro V., and Astore I.P.L. Method, technic and computations in the study of the trophic state of human scalp hair. J. Invest. Dermatol. 42 (1964) 421
7. Bevington P.R. Data Reduction and Error Analysis for the Physical Sciences (1969), McGraw-Hill Inc., New York 56
8. Brennan M. Changes in solubility, nonenzymatic glycation, and fluorescence of collagen in tail tendons from diabetic rats. J. Biol. Chem. 264 (1989) 20947
9. Brown T.R., Su B., Brown K.A., Schwartz M.A., Tobia A.M., and Kappler F. Modulation of in vivo 3-deoxyglucosone levels. Biochem. Soc. Trans. 31 (2003) 1433
10. Bunn H.F., Gabbay K.H., and Gallop P.M. The glycosylation of hemoglobin; relevance to diabetes mellitus. Science 200 (1978) 21
11. Chellan P., and Nagaraj R.H. Protein crosslinking by the Maillard reaction: dicarbonyl-derived imidazolium corsslinks in aging and diabetes. Arch. Biochem. Biophys. 368 (1999) 98
12. Chellan P., and Nagaraj R.H. Early glycation products produce pentosidine cross-links on native proteins. J. Biol. Chem. 276 (2001) 3895
13. Claffey D.J., and Ruth J.A. Amphetamine adducts of melanin intermediates demonstrated by matrix assisted laser desorpotion/ionization time-of-flight mass spectrometry. Chem. Res. Toxicol. 14 (2001) 1339
14. Colaco C.A., Ledesma M.D., Harrington C.R., and Avila J. The role of the Maillard reaction in other pathologies: Alzheimer's disease. Nephrol. Dial. Transplant. 11 (1996) 7 (Suppl)
15. Corman B., Duriez M., Poitevin P., Heudes D., Bruneval P., Tedgui A., and Levy B.I. Aminoguanidine prevents age-related arterial stiffening and cardiac hypertorophy. PNAS 95 (1998) 1301
16. Courtois M., Loussouarn G., Hourseau C., and Grollier J.F. Hair cycle and alopecia. Skin Pharmacol. 7 (1994) 84
17. Curtiss L.K., and Witztum J.L. Plasma apolipoproteins AI, AII, B CI, and E are glucosylated in hyperglycemic diabetic subjects. Diabetes 34 (1985) 452
18. David R., Leslie G., Beyan H., Sawtell P., Boehm B.O., Spector T.D., and Snieder H. Level of an advanced glycated end product is genetically determined. Diabetes 52 (2003) 2441
19. Dawber R. Cosmetic and medical causes of hair weathering. J. Cosmet. Dermatol. 1 (2002) 196
20. DCCT research group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N. Engl. J. Med. 329 (1993) 977
21. Derr R., Garret E., Stacy G.A., and Saudek C.D. Is HbA1c affected by glycemic instability?. Diabetes Care 26 (2003) 2728
22. Eser H.P., Pötsch L., Skopp G., and Moeller M.R. Influence of sample preparation on analytical results: drug analysis [GC/MS] on hair snippets versus hair powder using various extraction methods. Forensic Sci. Int. 84 (1997) 271
23. Fujimoto N., Yajima M., Ohnishi Y., Tajima S., Ishibashi A., Hata Y., Enomoto U., Konohana I., Wachi H., and Seyama Y. Advanced glycation end product-modified beta2-microglobulin is a component of amyloid fibrils of primary localized cutaneous nodular amyloidosis. J. Invest. Dermatol. 118 (2002) 479
24. Furth A.J. Methods for assaying nonenzymatic glycosylation. Anal. Biochem. 175 (1988) 347
25. Giardino T., Edelstein D., and Brownlee M. Nonenzymatic glycosylation in vitro and in bovine endothelial cells alters basic fibroblast growth factor activity. J. Clin. Invest. 94 (1994) 110
26. Gillespie J.M., and Marshall R.C. The proteins of normal and aberrant hair keratins. In: Orfanos C.E., Montagna W., and Stuttgen G. (Eds). Hair Research (1981), Springer-Verlag, Berlin 76
27. Gordon A., Glaser B., Wald M., Del Rio G., Della Casa L., Gross J., and Cerasi E. Glycosylated serum protein levels assayed with highly sensitive immunoradiometric assay accurately reflect glycemic control of diabetic patients. Diabetes Care 15 (1992) 645
28. Griffin E., Re A., Hamel N., Fu C., Bush H., McCaffrey T., and Asch A.S. A link between diabetes and atherosclerosis: glucose regulates expression of CD36 at the level of translation. Nat. Med. 7 7 (2001) 840
29. Gulmann C., Sheehan K.M., Kay E.W., Liotta L.A., and Petricoin III E.F. Array based proteomics: mapping of protein circuitries for diagnostics, prognostics, and therapy guidance in cancer. J. Pathol. 208 (2006) 595
30. Hollander M., and Wolfe D.A. Nonparametric Statistical Methods (1973), John Wiley and Sons, New York 147
31. Horiuchi S., Araki N., and Morino Y. Immunochemical approach to characterize advanced glycation end products of the Maillard reaction: evidence for the presence of a common structure. J. Biol. Chem. 266 (1991) 7329
32. Hummel M., Bonifacio E., Schmid S., Walter M., Knopff A., and Ziegler A.G. Early appearance of islet autoantibodies predicts childhood type 1 diabetes in offspring of diabetic parents. Ann. Intern. Med. 140 (2004) 882
33. Hutchinson P.E., and Thompson J.R. The cross sectional size and shape of human terminal scalp hair. Br. J. Dermatol. 136 (1997) 159
34. Ikeda K., Nagai R., Sakamoto T., Sano H., Araki T., Sakata N., Nakayama H., Yoshida M., Ueda S., and Horiuchi S. Immunochemical approaches to AGE-structures: characterization of anti-AGE antibodies. J. Immunol. Methods 215 (1998) 95
35. Itin P.H., and Fistarol S.K. Hair shaft abnormalities - clues to diagnosis and treatment. Dermatology 211 (2005) 63
36. James V.J., and Willis B.E. Molecular changes in skin predict predisposition to breast cancer. J. Med. Genet. 39 (2002) 1e
37. James V.J., Yue D.K., and McLennan S.V. Changes in the molecular structure of hair in insulin-dependent diabetes. Biochem. Biophys. Res. Commun. 233 (1997) 76
38. James V.J., Corino G., Robertson T., et al. Early diagnosis of breast cancer by hair diffraction. Int. J. Cancer 114 (2005) 969
39. James V.J., Richardson J.C., Robertson T.A., Papadimitriou J.M., Dutton N.S., Maley M.A.L., Berstein L.M., Lantseva O.E., and Martins R.N. Fibre diffraction of hair can provide a screening test for Alzheimer's Disease: a human and animal model study. Med. Sci. Monit. 11 (2005) CR53
40. Khawar S.L., Watson K., and Jones G.L. High resolution one-dimensional electrophoretic separation and partial characterization of human head hair proteins. Electrophoresis 16 (1995) 110
41. Kligman A.M. The human hair cycle. J. Invest. Dermatol. 33 (1959) 307
42. Kobayashi K., and Igimi H. Glycation index of hair for non-invasive estimation of diabetic control. Biol. Pharm. Bull. 19 (1996) 487
43. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680
44. Lin C.Y., Chen C.S., Shieh M.S., Wu C.H., and Lee H.M. Development of an automated immunoassay for advanced glycosylation end products in human serum. Clin. Biochem. 35 (2002) 189
45. Lo T.W.C., Westwood M.E., McLellan A.C., Selwood T., and Thornalley P.J. Binding and modification of proteins by methylglyoxal under physiological conditions. A kinetic and mechanistic study with N(alpha)-acetylarginine, N-acetylcysteine, N(alpha)-acetyl lysine and bovine serum albumin. J. Biol. Chem. 269 (1994) 32299
46. Madsen H., Ditzel J., and Hansen N. Hemoglobin A1c determinations in diabetic pregnancy. Diabetes Care 4 (1981) 541
47. Maillard L.C. Actions de acides amines sur les sucres. Formation de melanoidines par voie methodique. C. R. Acad. Sci. 154 (1912) 66
48. Mercer E.H. Some experiments on the orientation and hardening of keratin in the hair follicle. Biochim. Biophys. Acta 3 (1949) 161
49. Milner Y., Sudnik J., Filippi M., Kizoulis M., Kashgarian M., and Stenn K. Exogen, shedding phase of the hair growth cycle: characterization of a mouse model. J. Invest. Dermatol. 119 (2002) 639
50. Minamide L.S., and Bamburg J.R. A filter paper dye-binding assay for quantitative determination of protein without interference from reducing agents or detergents. Anal. Biochem. 190 (1990) 66
51. Mitsuhashi T., Vlassara H., Founds H.W., and Li Y.M. Standardizing the immunological measurement of advanced glycation endproducts using normal human serum. J. Immunol. Methods 207 (1997) 79
52. Miyata T., Ishiguro N., Yasuda Y., Ito T., Nangaku M., Iwata H., and Kurokawa K. Increased pentosidine, an advanced glycation end product, in plasma and synovial fluid from patients with rheumatoid arthritis and its relation with inflammatory markers. Biochem. Biophys. Res. Commun. 244 (1998) 45
53. Miyazawa N., and Uematsu T. Analysis of ofloxacin in hair as a measure of hair growth and as a time marker for hair analysis. Ther. Drug Monit. 14 (1992) 525
54. Monnier V.M., Sell D.A., Miyata S., and Nagaraj R.H. The Maillard reaction as a basis for a theory of aging. In: Finot P.A., et al. (Ed). The Maillard Reaction in Food Processing, Human Nutrition, and Physiology (1990), Birkhouser, Basel 393
55. Montagna W., and Van Scott E.J. The anatomy of the hair follicle. In: Montagna W., and Ellis R.A. (Eds). The Biology of Hair Growth (1958), Academic Press 39
56. Munch G., Schicktanz D., Behme A., Gerlach M., Biederer P., Palm D., and Schinzel R. Amino acid specificity of glycation and protein-AGE crosslinking reactivities determined with a dipeptide SPOT library. Nat. Biotechnol. 17 (1999) 1006
57. Nagai R., Horiuchi H., and Unno Y. Application of monoclonal antibody libraries for the measurement of glycation adducts. Biochem. Soc. Trans. 31 (2003) 1438
58. Nishikawa T., Edelstein D., Du X.-L., Yamagishi S., Matsumura T., Kaneda Y., Yorek M., Beebe D., Oates P., Hammes H.-P., Giardino I., and Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycemic damage. Nature 404 (2000) 787
59. Nissimov J. Normal head-hair length is correlated with its diameter. Clin. Exp. Dermatol. 29 (2004) 649
60. Nissimov J., and Elchalal U. Scalp hair diameter increases during pregnancy. Clin. Exp. Dermatol. 28 (2003) 525
61. Nissimov J., Milner Y., Ofan R., and Phillip M. Hair diameter of newly diagnosed insulin dependent diabetes mellitus (IDDM) patients decreases sharply prior to onset of the disease. In: Van Neste D., et al. (Ed). Hair Science and Technology (2003), Skinterface, Tournai 223
62. Paisey R.B., Clamp J.R., Kent M.J.C., Light N.D., Hopton M., and Hartog M. Glycosylation of hair. Possible measure of chronic hyperglycaemia. Br. Med. J. 288 (1984) 669
63. Paisey R.B., Lewin I.G., Hopton M., Frappel J., Roland J., and Turner G. Glycosylation of maternal hair and cord skin during pregnancy in diabetic and non-diabetic women. Diabet. Med. 2 (1985) 367
64. Paus R., and Cotsarelis G. The biology of hair follicles. N. Engl. J. Med. 341 (1999) 491
65. Pecoraro V., and Astore I.P.L. Measurements of hair growth under physiological conditions. In: Orfanos C.E., Montagna W., and Stüttgen G. (Eds). Hair Research, Status and Future Aspects (1990), Springer-Verlag, Berlin 237
66. Porter P.S., and Lobitz W.C. Human hair. a genetic marker. Br. J. Dermatol. 83 (1970) 225
67. Price V.H., Odom R.B., Ward R.B., and Jones F.T. Trichothiodystrophy. Sulfur-deficient brittle hair as a marker for a neuroectodermal symptom complex. Arch. Dermatol. 116 (1980) 1375
68. Raz I., Elias D., Avron A., Tamir M., Metzger M., and Cohen I.R. Beta-cell function in new-onset type 1 diabetes and immunomodulation with a heat-shock protein peptide (DiaPep277): a randomized, double-blind, phase II trial. Lancet 358 (2001) 1749
69. Reiser K.M. Nonenzymatic glycation of collagen in aging and diabetes. Exp. Biol. Med. 196 (1990) 17
70. Robbins C.R., and Robbins M.G. Scalp hair length. II. Estimating the percentages of adults in the USA and larger populations by hair length. J. Cosmet. Sci. 54 (2003) 367
71. Rockett J.C., Burczynski M.E., Fornace Jr. A.J., Herrmann P.C., Krawetz S.A., and Dix D.J. Surrogate tissue analysis: monitoring toxicant exposure and health status of inaccessible tissue s through the analysis of accessible tissues and cells. Toxicol. Appl. Pharmacol. 194 (2004) 189
72. Rohlfing C.L., Widmeyer H.-M., Little R.R., England J., Tennill A., and Goldstein D.E. Defining the relationship between plasma glucose and HbA1c. Diabetes Care 25 (2002) 275
73. Rushton D.H., James K.C., and Mortimer C.H. The unit area trichogram in the assessment of androgen-dependent alopecia. Br. J. Dermatol. 109 (1983) 429
74. Ryder M.L. Use of radioisotopes in the study of wool growth and fibre composition. Nature 178 (1956) 1409
75. Sachs H. History of hair analysis. Forensic Sci. Int. 84 (1997) 7
76. Schwertl M., Auerswald K., and Schnyder H. Reconstruction of the isotopic history of animal diets by hair segmental analysis. Rapid Commun. Mass Spectrom. 17 (2003) 1312
77. Sell D.R., Lapolla A., Odetti P., Fogarty J., and Monnier V.M. Pentosidine formation in skin correlates with severity of complications in individuals with long-standing insulin-dependent diabetes mellitus. Diabetes 41 (1992) 1286
78. Sell D.R., Lane M.A., Johnson W.A., Masoro E.J., Mock O.B., Reiser R.M., Fogarty J.F., Cutler R.G., Ingram D.K., Roth G.S., and Monnier V.M. Longevity and the genetic determination of collagen glycoxidation kinetics in mammalian senescence. PNAS 93 (1996) 485
79. Sell D.R., Kleinman N.R., and Monnier V.M. Longitudinal determination of skin collagen glycation and glycoxidation rates predicts early death in C57BL/6NDNIA mice. FASEB J. 14 (2000) 145
80. Sims R.T. The incorporation and fate of H3 tyrosine in the hair cortex of rats observed by radioautography. J. Cell Biol. 22 (1964) 403
81. Sims R.T. Beau's lines in hair. Reduction of hair shaft diameter associated with illness. Br. J. Dermatol. 79 (1967) 43
82. Stenn K.S., Parimoo S., and Prouty S. Growth of the hair follicle: a cycling and regenerating biological system. In: Chuong C.-M. (Ed). Molecular Basis of Epithelial Appendage Morphogenesis (1998), Landes, Austin, TX 111
83. Tarkka T., Yli-Mayry N., Mannermaa R.-M., Majamaa D., and Oikarinen J. Specific non-enzymatic glycation of the rat histone H1 nucleotide binding site in vitro in the presence of AlF4-A putative mechanism for impaired chromatin function. Biochim. Biophys. Acta 1180 (1993) 294
84. Thornalley P.J. Clinical significance of glycation. Clin. Lab. 45 (1999) 263
85. Thornalley P.J., Langborg A., and Minhas H.S. Formation of glyoxal methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem. J. 344 (1999) 109
86. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins form polyacrylamide gels to nitrocellulose sheets: procedures and some applications. PNAS 76 (1979) 4350
87. Van Scott E.J. Drug induced alopecia. In: Orfanos C.E., Montagna W., and Stüttgen G. (Eds). Hair Research, Status and Future Aspects (1981), Springer-Verlag, Berlin 469
88. Verbeke P., Perichon M., Borot-Laloi C., Schaeverbeke J., and Bakala H. Accumulation of advanced glycation endproducts in the rat nephron: link with circulating AGEs during aging. J. Histochem. Cytochem. 45 (1997) 1059
89. Vlassara H. Chronic diabetic complications and tissue glycosylation. Diabetes Care 13 (1990) 1180
90. Vlassara H., Bucala R., and Striker L. Biology of disease: pathogenic effects of advanced glycosylation: biochemical, biologic, and clinical implications for diabetes and aging. Lab. Invest. 70 (1994) 138
91. Williams D., Siock P., and Stenn K. 13-cis-retinoic acid affect sheath-shaft interaction of equine hair follicles in vitro. J. Invest. Dermatol. 106 (1996) 356
92. Yamauchi T., Kamon J., Waki H., Terauchi Y., Kubota N., Hara K., Mori Y., Ide T., Murakami K., Tsuboyama-Kasaoka N., Ezaki O., Akanuma Y., Gavrilova O., Vinson C., Reitman M.L., Kagechika H., Shudo K., Yoda M., Nakano Y., Tobe K., Nagai R., Kimura S., Tomita M., Froguel P., and Kadowaki T. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat. Med. 7 8 (2001) 941
93. Yu L., Robles D.T., Abiru N., Kaur P., Rewers M., Kelemen K., and Eisenbarth G.S. Early expression of antiinsulin autoantibodies of humans and the NOD mouse: evidence for early determination of subsequent diabetes. PNAS 97 (2000) 1701
94. Ziegler A.G., Hummel M., Schenker M., and Bonifacio E. Autoantibody appearance and risk for development of childhood diabetes in offspring of parents with type I diabetes: the 2-year analysis of the German BABYDIAB study. Diabetes 48 (1999) 460
95. Zisman A., Peroni O.D., Abel E.D., Michael M.D., Mauvais-Jarvis F., Lowell B.B., Wojtaszewski J.F., Hirshman M.F., Virkamaki A., Goodyear L.J., Kahn C.R., and Kahn B.B. Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat. Med. 6 (2000) 924