Advertisement

Journal of Chemical Ecology

, Volume 42, Issue 1, pp 33–39 | Cite as

The Effect of Ethnicity on Human Axillary Odorant Production

  • Katharine A. Prokop-Prigge
  • Kathryn Greene
  • Lauren Varallo
  • Charles J. Wysocki
  • George Preti
Article

Abstract

Previous findings from our laboratory highlighted marked ethnic differences in volatile organic compounds (VOCs) from cerumen among individuals of Caucasian, East Asian, and African-American descent, based, in part, on genetic differences in a gene that codes for a transport protein, which is a member of the ATP-binding cassette transporter, sub-family C, member 11 (ABCC11). In the current work, we hypothesized that axillary odorants produced by East Asians would differ markedly from those obtained from individuals of European or African descent based on the pattern of ethnic diversity that exists in ABCC11. Using gas chromatography/mass spectrometry (GC/MS) we examined differences in axillary odorant VOCs among 30 individuals of African-American, Caucasian, and East Asian descent with respect to their ABCC11 genotype. While no qualitative differences in the type of axillary odorants were observed across ethnic groups, we found that characteristic axillary odorants varied quantitatively with respect to ethnic origin. We propose that ABCC11 is not solely responsible for predicting the relative amounts of volatiles found in axillary secretions and that other biochemical pathways must be involved.

Keywords

Axillary odor Ethnicity/race Volatile organic compounds Genetics Analytical chemistry 

Notes

Acknowledgments

The authors thank Jason Eades for technical support. KAP acknowledges support from NIH-NIDCD Postdoctoral Training Grant 5T32DC0014 as well as Monell Institutional Funds. The genotyping was performed at the Monell Genotyping and DNA/RNA Analysis Core, which is supported, in part, by funding from the NIH-NIDCD Core Grant P30DC01173.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Akutsu T, Sekiguchi K, Ohmori T, Sakurada K (2006) Individual comparisons of the levels of (E)-3-methyl-2-hexenoic acid, an axillary odor-related compound, in Japanese. Chem Senses 31:557–563CrossRefPubMedGoogle Scholar
  2. Annigan J (2014) Foods that are highest in isoleucine & leucine. http://www.livestrong.com/article/275274-foods-that-are-highest-in-isoleucine-leucine/. Accessed 24 October 2014
  3. Barzantny H, Brune I, Tauch A (2012) Molecular basis of human body odour formation: insights deduced from corynebacterial genome sequences. Int J Cosmet Sci 34:2–11CrossRefPubMedGoogle Scholar
  4. Baumann T, Bergmann S, Schmidt-Rose T, Max H, Martin A, Enthaler B, Terstegen L, Schweiger D, Kalbacher H, Wenck H, et al. (2014) Glutathione-conjugated sulfanylalkanols are substrates for ABCC11 and gamma-glutamyl transferase 1: a potential new pathway for the formation of odorant precursors in the apocrine sweat gland. Exp Dermatol 23:247–252PubMedCentralCrossRefPubMedGoogle Scholar
  5. Bird S, Gower DB (1981) The validation and use of a radioimmunoassay for 5 alpha-androst-16-en-3-one in human axillary collections. J Steroid Biochem 14:213–219CrossRefPubMedGoogle Scholar
  6. Chen ZS, Guo Y, Belinsky MG, Kotova E, Kruh GD (2005) Transport of bile acids, sulfated steroids, estradiol 17-beta-D-glucuronide, and leukotriene C4 by human multidrug resistance protein 8 (ABCC11). Mol Pharmacol 67:545–557CrossRefPubMedGoogle Scholar
  7. Dormont L, Bessiere JM, Cohuet A (2013) Human skin volatiles: a review. J Chem Ecol 39(5):569–578CrossRefPubMedGoogle Scholar
  8. Gallagher M, Wysocki CJ, Leyden JJ, Spielman AI, Sun X, Preti G (2008) Analyses of volatile organic compounds from human skin. Br J Dermatol 159:780–791PubMedCentralCrossRefPubMedGoogle Scholar
  9. Green ED, Guyer MS, et al. (2011) Charting a course for genomic medicine from base pairs to bedside. Nature 470:204–213CrossRefPubMedGoogle Scholar
  10. Harker M, Carvell AM, Marti VP, Riazanskaia S, Kelso H, Taylor D, Grimshaw S, Arnold DS, Zillmer R, Shaw J, et al. (2014) Functional characterisation of a SNP in the ABCC11 allele - effects on axillary skin metabolism, odour generation and associated behaviours. J Dermatol Sci 73:23–30CrossRefPubMedGoogle Scholar
  11. Hasegawa Y, Yabuki M, Matsukane M (2004) Identification of new odoriferous compounds in human axillary sweat. Chem Biodivers 1:2042–2050CrossRefPubMedGoogle Scholar
  12. Havlicek J, Lenochova P (2006) The effect of meat consumption on body odor attractiveness. Chem Senses 31:747–752CrossRefPubMedGoogle Scholar
  13. Inoue Y, Mori T, Toyoda Y, Sakurai A, Ishikawa T, Mitani Y, Hayashizaki Y, Yoshimura Y, Kurahashi H, Sakai Y (2010) Correlation of axillary osmidrosis to a SNP in the ABCC11 gene determined by the smart amplification process (SmartAmp) method. J Plast Reconstr Aesthet Surg 63:1369–1374CrossRefPubMedGoogle Scholar
  14. Jacoby RB, Brahms JC, Ansari SA, Mattai J (2004) Detection and quantification of apocrine secreted odor-binding protein on intact human axillary skin. Int J Cosmet Sci 26:37–46CrossRefPubMedGoogle Scholar
  15. Kruh GD, Guo Y, Hopper-Borge E, Belinsky MG, Chen ZS (2007) ABCC10, ABCC11, and ABCC12. Pflugers Arch 453:675–684CrossRefPubMedGoogle Scholar
  16. Labows JN, Preti G, Hoelzle E, Leyden J, Kligman A (1979) Steroid analysis of human apocrine secretion. Steroids 34:249–258CrossRefPubMedGoogle Scholar
  17. Leyden JJ, McGinley KJ, Holzle E, Labows JN, Kligman AM (1981) The microbiology of the human axilla and its relationship to axillary odor. J Investig Dermatol 77:413–416CrossRefPubMedGoogle Scholar
  18. Martin A, Saathoff M, Kuhn F, Max H, Terstegen L, Natsch A (2010) A functional ABCC11 allele is essential in the biochemical formation of human axillary odor. J Investig Dermatol 130:529–540CrossRefPubMedGoogle Scholar
  19. Nakano M, Miwa N, Hirano A, Yoshiura K, Niikawa N (2009) A strong association of axillary osmidrosis with the wet earwax type determined by genotyping of the ABCC11 gene. BMC Genet 10:42PubMedCentralCrossRefPubMedGoogle Scholar
  20. Natsch A (2015) What makes us smell: the biochemistry of body odour and the design of new deodorant ingredients. Chimia 69:414–420CrossRefPubMedGoogle Scholar
  21. Natsch A, Gfeller H, Gygax P, Schmid J, Acuna G (2003) A specific bacterial aminoacylase cleaves odorant precursors secreted in the human axilla. J Biol Chem 278:5718–5727CrossRefPubMedGoogle Scholar
  22. Natsch A, Schmid J, Flachsmann F (2004) Identification of odoriferous sulfanylalkanols in human axilla secretions and their formation through cleavage of cysteine precursors by a C-S lyase isolated from axilla bacteria. Chem Biodivers 1:1058–1072CrossRefPubMedGoogle Scholar
  23. Natsch A, Derrer S, Flachsmann F, Schmid J (2006) A broad diversity of volatile carboxylic acids, released by a bacterial aminoacylase from axilla secretions, as candicate molecules for the determination of human-body odor type. Chem Biodivers 3:1–20CrossRefPubMedGoogle Scholar
  24. Pierce Jr JD, Zeng XN, Aronov EV, Preti G, Wysocki CJ (1995) Cross-adaptation of sweaty-smelling 3-methyl-2-hexenoic acid by a structurally-similar, pleasant-smelling odorant. Chem Senses 20:401–411Google Scholar
  25. Preti G, Leyden JJ (2010) Genetic influences on human body odor: from genes to the axillae. J Investig Dermatol 130:344–346CrossRefPubMedGoogle Scholar
  26. Preti G, Wysocki CJ, Barnhart KT, Sondheimer SJ, Leyden JJ (2003) Male axillary extracts contain pheromones that affect pulsatile secretion of luteinizing hormone and mood in women recipients. Biol Reprod 68:2107–2113CrossRefPubMedGoogle Scholar
  27. ProCon.org (2010) Lactose intolorance by ethnicity and region. http://milk.procon.org/view.resource.php?resourceID=000661. Accessed 24 October 2014
  28. Prokop-Prigge KA, Thaler E, Wysocki CJ, Preti G (2014) Identification of volatile organic compounds in human cerumen. J Chromatogr B 953-954:48–52CrossRefGoogle Scholar
  29. Prokop-Prigge KA, Mansfield CJ, Parker MR, Thaler E, Grice EA, Wysocki CJ, Preti G (2015) Ethnic/racial and genetic influences on cerumen odorant profiles. J Chem Ecol 41:67–74PubMedCentralCrossRefPubMedGoogle Scholar
  30. Spielman AI, Zeng XN, Leyden JJ, Preti G (1995) Proteinaceous precursors of human axillary odor: isolation of two novel odor-binding proteins. Experientia 51:40–47PubMedGoogle Scholar
  31. Spielman AI, Sunavala G, Harmony JA, Stuart WD, Leyden JJ, Turner G, Vowels BR, Lam WC, Yang S, Preti G (1998) Identification and immunohistochemical localization of protein precursors to human axillary odors in apocrine glands and secretions. Arch Dermatol 134:813–818CrossRefPubMedGoogle Scholar
  32. Starkenmann C, Niclass Y, Troccaz M, Clark AJ (2005) Identification of the precursor of (S)-3-methyl-3-sulfanylhexan-1-ol, the sulfury malodour of human axilla sweat. Chem Biodivers 2:705–715CrossRefPubMedGoogle Scholar
  33. Toyoda Y, Sakurai A, Mitani Y, Nakashima M, Yoshiura K, Nakagawa H, Sakai Y, Ota I, Lezhava A, Hayashizaki Y, et al. (2009) Earwax, osmidrosis, and breast cancer: why does one SNP (538G > a) in the human ABC transporter ABCC11 gene determine earwax type? FASEB J 23:2001–2013CrossRefPubMedGoogle Scholar
  34. Troccaz M, Starkenmann C, Niclass Y, van de Waal M, Clark AJ (2004) 3-methyl-3-sulfanylhexan-1-ol as a major descriptor for the human axilla-sweat odour profile. Chem Biodivers 1:1022–1035CrossRefPubMedGoogle Scholar
  35. Troccaz M, Borchard G, Vuilleumier C, et al. (2009) Gender-specific differences between the concentrations of nonvolatile (R)/(S)-3-methyl-3-sulfanylhexan-1-Ol and (R)/(S)-3-hydroxy-3-methyl-hexanoic acid odor precursors in axillary secretions. Chem Senses 34:203–210CrossRefPubMedGoogle Scholar
  36. Wedekind C, Seebeck T, Bettens F, Paepke AJ (1995) MHC-dependent mate preferences in humans. Proc Biol Sci 260:245–249CrossRefPubMedGoogle Scholar
  37. Yoshiura K, Kinoshita A, Ishida T, Ninokata A, Ishikawa T, Kaname T, Bannai M, Tokunaga K, Sonoda S, Komaki R, et al. (2006) A SNP in the ABCC11 gene is the determinant of human earwax type. Nat Genet 38:324–330CrossRefPubMedGoogle Scholar
  38. Zeng XN, Preti G, Leyden JJ, Lawley HJ, Sawano K, Nohara I (1991) Analysis of the characteristic odors from the male axillae. J Chem Ecol 17:1469–1492CrossRefPubMedGoogle Scholar
  39. Zeng XN, Leyden JJ, Brand JG, Spielman AI, McGinley KJ, Preti G (1992) An investigation of human apocrine gland secetion for axillary odor precursors. J Chem Ecol 18:1039–1055CrossRefPubMedGoogle Scholar
  40. Zeng C, Spielman AI, Vowels BR, Leyden JJ, Biemann K, Preti G (1996a) A human axillary odorant is carried by apolipoprotein D. Proc Natl Acad Sci U S A 93:6626–6630PubMedCentralCrossRefPubMedGoogle Scholar
  41. Zeng XN, Leyden JJ, Spielman AI, Preti G (1996b) Analysis of characteristic human female axillary odors: qualitative comparison to males. J Chem Ecol 22:237–257CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Monell Chemical Senses CenterPhiladelphiaUSA
  2. 2.School of Veterinary MedicineUniversity of PennsylvaniaPhiladelphiaUSA
  3. 3.Department of Dermatology, Perelman School of MedicineUniversity of PennsylvaniaPhiladelphiaUSA

Personalised recommendations