Biological Trace Element Research

, Volume 137, Issue 1, pp 23–39 | Cite as

Chromium III Histidinate Exposure Modulates Gene Expression in HaCaT Human Keratinocytes Exposed to Oxidative Stress

  • Florence Hazane-Puch
  • Rachida Benaraba
  • Kita Valenti
  • Mireille Osman
  • François Laporte
  • Alain Favier
  • Richard A. Anderson
  • Anne-Marie Roussel
  • Isabelle Hininger-Favier
Article

Abstract

While the toxicity of hexavalent chromium is well established, trivalent chromium is an essential nutrient involved in insulin and glucose homeostasis. To study the antioxidant effects of Cr(III)His, cDNA arrays were used to investigate the modulation of gene expression by trivalent chromium histidinate (Cr(III)His) in HaCaT human keratinocytes submitted to hydrogen peroxide (H2O2). Array was composed by a set of 81 expressed sequences tags (ESTs) essentially represented by antioxidant and DNA repair genes. HaCaT were preincubated for 24 h with 50 μM Cr(III)His and were treated with 50 μM H2O2. Total RNAs were isolated immediately or 6 h after the stress. In Cr(III)His preincubated cells, transcripts related to antioxidant family were upregulated (glutathione synthetase, heme oxygenase 2, peroxiredoxin 4). In Cr(III)His preincubated cells and exposed to H2O2, increased expressions of polymerase delta 2 and antioxidant transcripts were observed. Biochemical methods performed in parallel to measure oxidative stress in cells showed that Cr(III)His supplementation before H2O2 stress protected HaCaT from thiol groups decrease and thiobarbituric acid reactive substances increase. In summary, these results give evidence of antioxidant gene expression and antioxidant protection in HaCaT preincubated with Cr(III)His and help to explain the lack of toxicity reported for Cr(III)His.

Keywords

Oxidative stress Hydrogen peroxide Cr(III)His supplementation Gene expression HaCaT TBARS Thiol groups 

Abbreviations

8-oxodGuo

8-Oxo-7-8-dihydro-2′-deoxyguanosine

ACTB

Actin, beta

ANOVA

Analysis of variance

Cr

Chromium

Cr(III)

Trivalent chromium

Cr(III)His

Trivalent chromium histidinate

Cr(VI)

Hexavalent chromium

DMSO

Dimethylsulfoxide

DTNB

5,5′-Dithio-Bis (2-nitrobenzoic acid)

ECM

Extracellular matrix

ESTs

Expressed sequence tags

GADD45A

Growth arrest and DNA-damage-inducible alpha

GAPDH

Glyceraldehyde-3-phosphate dehydrogenase

GCLM

Glutamate-cysteine ligase, modifier subunit

GPX1

Glutathione peroxidase 1

GSH

Glutathione

GSR

Glutathione reductase

GSS

Glutathione synthetase

GST

Glutathione S-transferase

H2O2

Hydrogen peroxide

HMOX2

Heme oxygenase 2

IKBIA

Nuclear factor of kappa light polypeptide gene enhancer in B-cells inhibitor, alpha

MMP2

Matrix metallopeptidase 2

MTT

3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide

NAC

N-acetyl cysteine

NER

Nucleotide excision repair

NFKB1

Nuclear factor of kappa light polypeptide gene enhancer in B-cells 1

NHEJ

Non-homologous end-joining

PBS

Phosphate-buffered saline

PCR

Polymerase chain reaction

PLA2G5

Phospholipase A2, group V

POLD2

Polymerase delta 2

PRDX4

Peroxiredoxin 4

ROS

Reactive oxygen species

RPL32

Ribosomal protein L32

SE

Standard error

-SH

Thiol groups

SHC1

Src homology 2 domain containing transforming protein 1

SOD1

Superoxide dismutase 1

TBARS

Thiobarbituric acid reactive substances

TXN

Thioredoxin

XPC

Xeroderma pigmentosum C

Notes

Acknowledgements

This study was part of a US Department of Agriculture funded study entitled “Insulin potentiating compounds and antioxidant nutrients in the prevention and alleviation of glucose intolerance and diabetes” and the International Agreement between laboratories from Joseph Fourier University, Grenoble, France and the Beltsville Human Nutrition Research Center entitled “Naturally Occurring Insulin Enhancing Factors”.

References

  1. 1.
    Anderson RA (1997) Nutritional factors influencing the glucose/insulin system: chromium. J Am Coll Nutr 16:404–410PubMedGoogle Scholar
  2. 2.
    Chromium ARA (1998) Glucose intolerance and diabetes. J Am Coll Nutr 17:548–555Google Scholar
  3. 3.
    Sugiyama M, Tsuzuki K, Ogura R (1991) Effect of ascorbic acid on DNA damage, cytotoxicity, glutathione reductase, and formation of paramagnetic chromium in Chinese hamster V-79 cells treated with sodium chromate(VI). J Biol Chem 266:3383–3386PubMedGoogle Scholar
  4. 4.
    Martin J, Wang ZQ, Zhang XH, Wachtel D, Volaufova J, Matthews DE, Cefalu WT (2006) Chromium picolinate supplementation attenuates body weight gain and increases insulin sensitivity in subjects with type 2 diabetes. Diabetes Care 29:1826–1832CrossRefPubMedGoogle Scholar
  5. 5.
    Anton SD, Morrison CD, Cefalu WT, Martin CK, Coulon S, Geiselman P, Han H, White CL, Williamson DA (2008) Effects of chromium picolinate on food intake and satiety. Diabetes Technol Ther 10:405–412CrossRefPubMedGoogle Scholar
  6. 6.
    De Flora S, Camoirano A, Bagnasco M, Bennicelli C, Corbett GE, Kerger BD (1997) Estimates of the chromium(VI) reducing capacity in human body compartments as a mechanism for attenuating its potential toxicity and carcinogenicity. Carcinogenesis 18:531–537CrossRefPubMedGoogle Scholar
  7. 7.
    Shi X, Dalal NS, Kasprzak KS (1993) Generation of free radicals from hydrogen peroxide and lipid hydroperoxides in the presence of Cr(III). Arch Biochem Biophys 302:294–299CrossRefPubMedGoogle Scholar
  8. 8.
    Voitkun V, Zhitkovich A, Costa M (1998) Cr(III)-mediated crosslinks of glutathione or amino acids to the DNA phosphate backbone are mutagenic in human cells. Nucleic Acids Res 26:2024–2030CrossRefPubMedGoogle Scholar
  9. 9.
    Anderson RA, Roussel AM, Zouari N, Mahjoub S, Matheau JM, Kerkeni A (2001) Potential antioxidant effects of zinc and chromium supplementation in people with type 2 diabetes mellitus. J Am Coll Nutr 20:212–218PubMedGoogle Scholar
  10. 10.
    De Flora S, Bagnasco M, Serra D, Zanacchi P (1990) Genotoxicity of chromium compounds. A review. Mutat Res 238:99–172PubMedGoogle Scholar
  11. 11.
    Cheng HH, Lai MH, Hou WC, Huang CL (2004) Antioxidant effects of chromium supplementation with type 2 diabetes mellitus and euglycemic subjects. J Agric Food Chem 52:1385–1389CrossRefPubMedGoogle Scholar
  12. 12.
    Hininger I, Benaraba R, Osman M, Faure H, Marie Roussel A, Anderson RA (2007) Safety of trivalent chromium complexes: no evidence for DNA damage in human HaCaT keratinocytes. Free Radic Biol Med 42:1759–1765CrossRefPubMedGoogle Scholar
  13. 13.
    Cheng RY, Alvord WG, Powell D, Kasprzak KS, Anderson LM (2002) Microarray analysis of altered gene expression in the TM4 Sertoli-like cell line exposed to chromium(III) chloride. Reprod Toxicol 16:223–236CrossRefPubMedGoogle Scholar
  14. 14.
    Hazane F, Valenti K, Sauvaigo S, Peinnequin A, Mouret C, Favier A, Beani JC (2005) Ageing effects on the expression of cell defence genes after UVA irradiation in human male cutaneous fibroblasts using cDNA arrays. J Photochem Photobiol B 79:171–190CrossRefPubMedGoogle Scholar
  15. 15.
    Ermolli M, Menne C, Pozzi G, Serra MA, Clerici LA (2001) Nickel, cobalt and chromium-induced cytotoxicity and intracellular accumulation in human hacat keratinocytes. Toxicology 159:23–31CrossRefPubMedGoogle Scholar
  16. 16.
    Horowitz SB, Finley BL (1994) Setting health-protective soil concentrations for dermal contact allergens: a proposed methodology. Regul Toxicol Pharmacol 19:31–47CrossRefPubMedGoogle Scholar
  17. 17.
    BN ARA, Polansky MM, Gautschi K (1996) Dietary chromium effects on tissue chromium concentrations and chromium absorption in rats. Journal Trace Elements Exp Med 9:11–25CrossRefGoogle Scholar
  18. 18.
    Anderson RA, Polansky MM, Bryden NA (2004) Stability and absorption of chromium and absorption of chromium histidinate complexes by humans. Biol Trace Elem Res 101:211–218CrossRefPubMedGoogle Scholar
  19. 19.
    Gusnanto A, Calza S, Pawitan Y (2007) Identification of differentially expressed genes and false discovery rate in microarray studies. Curr Opin Lipidol 18:187–193CrossRefPubMedGoogle Scholar
  20. 20.
    Lafond PF (1995) Measurement of plasma sulfhydryl and carbonyl groups as a possible indicator of protein oxidation. In Analysis of Free Radical in Biological Systems. Birkhauser Verlag, Switzerland 237–248Google Scholar
  21. 21.
    Richard MJ, Guiraud P, Meo J, Favier A (1992) High-performance liquid chromatographic separation of malondialdehyde-thiobarbituric acid adduct in biological materials (plasma and human cells) using a commercially available reagent. J Chromatogr 577:9–18CrossRefPubMedGoogle Scholar
  22. 22.
    Johnson F, Giulivi C (2005) Superoxide dismutases and their impact upon human health. Mol Aspects Med 26:340–352CrossRefPubMedGoogle Scholar
  23. 23.
    Forman HJ, Dickinson DA (2003) Oxidative signaling and glutathione synthesis. Biofactors 17:1–12CrossRefPubMedGoogle Scholar
  24. 24.
    Lee KM, Lee JG, Seo EY, Lee WH, Nam YH, Yang JM, Kee SH, Seo YJ, Park JK, Kim CD, Lee JH (2005) Analysis of genes responding to ultraviolet B irradiation of HaCaT keratinocytes using a cDNA microarray. Br J Dermatol 152:52–59CrossRefPubMedGoogle Scholar
  25. 25.
    Sesto A, Navarro M, Burslem F, Jorcano JL (2002) Analysis of the ultraviolet B response in primary human keratinocytes using oligonucleotide microarrays. Proc Natl Acad Sci U S A 99:2965–2970CrossRefPubMedGoogle Scholar
  26. 26.
    Kahari VM, Saarialho-Kere U (1997) Matrix metalloproteinases in skin. Exp Dermatol 6:199–213CrossRefPubMedGoogle Scholar
  27. 27.
    Toy LW (2005) Matrix metalloproteinases: their function in tissue repair. J Wound Care 14:20–22PubMedGoogle Scholar
  28. 28.
    Araki M, Masutani C, Takemura M, Uchida A, Sugasawa K, Kondoh J, Ohkuma Y, Hanaoka F (2001) Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair. J Biol Chem 276:18665–18672CrossRefPubMedGoogle Scholar
  29. 29.
    Brooks PJ, Wise DS, Berry DA, Kosmoski JV, Smerdon MJ, Somers RL, Mackie H, Spoonde AY, Ackerman EJ, Coleman K, Tarone RE, Robbins JH (2000) The oxidative DNA lesion 8, 5′-(S)-cyclo-2′-deoxyadenosine is repaired by the nucleotide excision repair pathway and blocks gene expression in mammalian cells. J Biol Chem 275:355–362Google Scholar
  30. 30.
    Kuraoka I, Bender C, Romieu A, Cadet J, Wood RD, Lindahl T (2000) Removal of oxygen free-radical-induced 5′, 8-purine cyclodeoxynucleosides from DNA by the nucleotide excision-repair pathway in human cells. Proc Natl Acad Sci U S A 97:3832–3837CrossRefPubMedGoogle Scholar
  31. 31.
    D'Errico M, Parlanti E, Teson M, de Jesus BM, Degan P, Calcagnile A, Jaruga P, Bjoras M, Crescenzi M, Pedrini AM, Egly JM, Zambruno G, Stefanini M, Dizdaroglu M, Dogliotti E (2006) New functions of XPC in the protection of human skin cells from oxidative damage. Embo J 25:4305–4315CrossRefPubMedGoogle Scholar
  32. 32.
    Jin DY, Chae HZ, Rhee SG, Jeang KT (1997) Regulatory role for a novel human thioredoxin peroxidase in NF-kappaB activation. J Biol Chem 272:30952–30961CrossRefPubMedGoogle Scholar
  33. 33.
    Anderson MT, Staal FJ, Gitler C, Herzenberg LA, Herzenberg LA (1994) Separation of oxidant-initiated and redox-regulated steps in the NF-kappa B signal transduction pathway. Proc Natl Acad Sci U S A 91:11527–11531CrossRefPubMedGoogle Scholar
  34. 34.
    Baeuerle PA, Henkel T (1994) Function and activation of NF-kappa B in the immune system. Annu Rev Immunol 12:141–179PubMedGoogle Scholar
  35. 35.
    Isoir M, Buard V, Gasser P, Voisin P, Lati E, Benderitter M (2006) Human keratinocyte radiosensitivity is linked to redox modulation. J Dermatol Sci 41:55–65CrossRefPubMedGoogle Scholar
  36. 36.
    Pandolfi S, Bonafe M, Di Tella L, Tiberi L, Salvioli S, Monti D, Sorbi S, Franceschi C (2005) p66(shc) is highly expressed in fibroblasts from centenarians. Mech Ageing Dev 126:839–844CrossRefPubMedGoogle Scholar
  37. 37.
    Purdom S, Chen QM (2003) p66(Shc): at the crossroad of oxidative stress and the genetics of aging. Trends Mol Med 9:206–210CrossRefPubMedGoogle Scholar
  38. 38.
    Yu BP, Chung HY (2006) Adaptive mechanisms to oxidative stress during aging. Mech Ageing Dev 127:436–443PubMedGoogle Scholar
  39. 39.
    Migliaccio E, Giorgio M, Mele S, Pelicci G, Reboldi P, Pandolfi PP, Lanfrancone L, Pelicci PG (1999) The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 402:309–313CrossRefPubMedGoogle Scholar
  40. 40.
    Migliaccio E, Giorgio M, Pelicci PG (2006) Apoptosis and aging: role of p66Shc redox protein. Antioxid Redox Signal 8:600–608CrossRefPubMedGoogle Scholar
  41. 41.
    Stevenson MA, Pollock SS, Coleman CN, Calderwood SK (1994) X-irradiation, phorbol esters, and H2O2 stimulate mitogen-activated protein kinase activity in NIH-3T3 cells through the formation of reactive oxygen intermediates. Cancer Res 54:12–15PubMedGoogle Scholar
  42. 42.
    Zhao L, Chang LS (1997) The human POLD1 gene. Identification of an upstream activator sequence, activation by Sp1 and Sp3, and cell cycle regulation. J Biol Chem 272:4869–4882CrossRefPubMedGoogle Scholar
  43. 43.
    Hubscher U, Nasheuer HP, Syvaoja JE (2000) Eukaryotic DNA polymerases, a growing family. Trends Biochem Sci 25:143–147CrossRefPubMedGoogle Scholar
  44. 44.
    Snow ET, Xu LS (1991) Chromium(III) bound to DNA templates promotes increased polymerase processivity and decreased fidelity during replication in vitro. Biochemistry 30:11238–11245CrossRefPubMedGoogle Scholar
  45. 45.
    O'Brien TJ, Brooks BR, Patierno SR (2005) Nucleotide excision repair functions in the removal of chromium-induced DNA damage in mammalian cells. Mol Cell Biochem 279:85–95CrossRefPubMedGoogle Scholar
  46. 46.
    Snow ET (1994) Effects of chromium on DNA replication in vitro. Environ Health Perspect 102(Suppl 3):41–44CrossRefPubMedGoogle Scholar
  47. 47.
    Patlolla AK, Barnes C, Yedjou C, Velma VR, Tchounwou PB (2009) Oxidative stress, DNA damage, and antioxidant enzyme activity induced by hexavalent chromium in Sprague-Dawley rats. Environ Toxicol 24:66–73CrossRefPubMedGoogle Scholar
  48. 48.
    Bencheikh-Latmani R, Obraztsova A, Mackey MR, Ellisman MH, Tebo BM (2007) Toxicity of Cr(lll) to Shewanella sp. strain MR-4 during Cr(VI) reduction. Environ Sci Technol 41:214–220CrossRefPubMedGoogle Scholar
  49. 49.
    Roling JA, Baldwin WS (2006) Alterations in hepatic gene expression by trivalent chromium in Fundulus heteroclitus. Mar Environ Res 62(Suppl):S122–S127CrossRefPubMedGoogle Scholar
  50. 50.
    Tezuka M, Momiyama K, Edano T, Okada S (1991) Protective effect of chromium(III) on acute lethal toxicity of carbon tetrachloride in rats and mice. J Inorg Biochem 42:1–8CrossRefPubMedGoogle Scholar

Copyright information

© Humana Press Inc. 2009

Authors and Affiliations

  • Florence Hazane-Puch
    • 1
  • Rachida Benaraba
    • 2
  • Kita Valenti
    • 1
  • Mireille Osman
    • 2
    • 3
  • François Laporte
    • 1
  • Alain Favier
    • 1
  • Richard A. Anderson
    • 4
  • Anne-Marie Roussel
    • 2
    • 3
  • Isabelle Hininger-Favier
    • 2
    • 3
    • 5
  1. 1.Département de Biologie Intégrée, Biologie NutritionnelleCentre Hospitalier UniversitaireGrenoble Cedex 09France
  2. 2.LBFAUniversité Joseph FourierGrenoble IFrance
  3. 3.INSERM, U884GrenobleFrance
  4. 4.USDA, ARS, BHNRC, DGILBeltsvilleUSA
  5. 5.LBFA (Laboratoire de Bioénergétique Fondamentale et Appliquée)UFR PharmacieLa TroncheFrance

Personalised recommendations