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Published in: Archives of Dermatological Research 1/2013

01-01-2013 | Original Paper

Chemoprevention of doxorubicin-induced alopecia in mice by dietary administration of l-cystine and vitamin B6

Authors: Francesco D’Agostini, Paolo Fiallo, Massimo Ghio, Silvio De Flora

Published in: Archives of Dermatological Research | Issue 1/2013

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Abstract

Chemotherapy-induced hair loss is one of the most serious and feared adverse effects of cancer therapy. Almost all traditional chemotherapeutic agents induce a more or less severe alopecia. At present, there is no effective treatment capable of preventing this damage. Several different experimental approaches, using various animal models, have been investigated over the last years, with promising results. Sulphur-containing amino acids (cystine, cysteine) are essential components for the health of normal hair. l-Cystine is used in the treatment of various forms of alopecia. Vitamin B6 plays an important role in the development and maintenance of the skin and it is useful in reducing hair loss. In the present study, we demonstrated that the combined oral administration at high dosages of l-cystine (1,600 or 800 mg/kg body weight/day) and vitamin B6 (160 or 80 mg/kg body weight/day) is an effective chemopreventive treatment against alopecia induced by doxorubicin treatment (1.1 mg/kg body weight intravenously) in C57BL/6 mice.
Literature
1.
go back to reference Amoh Y, Li L, Yang M, Moossa AR, Katsuoka K, Penman S, Hoffman RM (2004) Nascent blood vessels in the skin arise from nestin-expressing hair-follicle cells. PNAS USA 101:13291–13295PubMedCrossRef Amoh Y, Li L, Yang M, Moossa AR, Katsuoka K, Penman S, Hoffman RM (2004) Nascent blood vessels in the skin arise from nestin-expressing hair-follicle cells. PNAS USA 101:13291–13295PubMedCrossRef
2.
go back to reference Amoh Y, Li L, Yang M, Jiang P, Moossa AR, Katsuoka K, Hoffman RM (2005) Hair follicle-derived blood vessels vascularize tumors in skin and are inhibited by doxorubicin. Cancer Res 65:2337–2343PubMedCrossRef Amoh Y, Li L, Yang M, Jiang P, Moossa AR, Katsuoka K, Hoffman RM (2005) Hair follicle-derived blood vessels vascularize tumors in skin and are inhibited by doxorubicin. Cancer Res 65:2337–2343PubMedCrossRef
3.
go back to reference Amoh Y, Li L, Katsuoka K, Hoffman RM (2007) Chemotherapy targets the hair follicle vascular network but not the stem cells. J Invest Dermatol 127:11–15PubMedCrossRef Amoh Y, Li L, Katsuoka K, Hoffman RM (2007) Chemotherapy targets the hair follicle vascular network but not the stem cells. J Invest Dermatol 127:11–15PubMedCrossRef
4.
go back to reference Anand SS (2005) Protective effect of vitamin B6 in chromium-induced oxidative stress in liver. J Appl Toxicol 25:440–443PubMedCrossRef Anand SS (2005) Protective effect of vitamin B6 in chromium-induced oxidative stress in liver. J Appl Toxicol 25:440–443PubMedCrossRef
5.
go back to reference Aoshiba K, Yasui S, Nishimura K, Nagai A (1999) Thiol depletion induces apoptosis in cultured lung fibroblasts. Am J Respir Cell Mol Biol 21:54–64PubMed Aoshiba K, Yasui S, Nishimura K, Nagai A (1999) Thiol depletion induces apoptosis in cultured lung fibroblasts. Am J Respir Cell Mol Biol 21:54–64PubMed
6.
go back to reference Ardestani A, Yazdanparast R, Nejad AS (2008) 2-Deoxy-d-ribose-induced oxidative stress causes apoptosis in human monocytic cells: prevention by pyridoxal-5′-phosphate. Toxicol In Vitro 22:968–979PubMedCrossRef Ardestani A, Yazdanparast R, Nejad AS (2008) 2-Deoxy-d-ribose-induced oxidative stress causes apoptosis in human monocytic cells: prevention by pyridoxal-5′-phosphate. Toxicol In Vitro 22:968–979PubMedCrossRef
7.
go back to reference Baden HP, Kubilus J (1980) Analysis of hair from alopecia congenita. J Am Acad Dermatol 3:623–626PubMedCrossRef Baden HP, Kubilus J (1980) Analysis of hair from alopecia congenita. J Am Acad Dermatol 3:623–626PubMedCrossRef
8.
go back to reference Balsari AL, Morelli D, Ménard S, Veronesi U, Colnaghi MI (1994) Protection against doxorubicin-induced alopecia in rats by liposome-entrapped monoclonal antibodies. FASEB J 8:226–230PubMed Balsari AL, Morelli D, Ménard S, Veronesi U, Colnaghi MI (1994) Protection against doxorubicin-induced alopecia in rats by liposome-entrapped monoclonal antibodies. FASEB J 8:226–230PubMed
9.
go back to reference Banjac A, Perisic T, Sato H, Seiler A, Bannai S, Weiss N, Kölle P, Tschoep K, Issels RD, Daniel PT, Conrad M, Bornkamm GW (2008) The cystine/cysteine cycle: a redox cycle regulating susceptibility versus resistance to cell death. Oncogene 27:1618–1628PubMedCrossRef Banjac A, Perisic T, Sato H, Seiler A, Bannai S, Weiss N, Kölle P, Tschoep K, Issels RD, Daniel PT, Conrad M, Bornkamm GW (2008) The cystine/cysteine cycle: a redox cycle regulating susceptibility versus resistance to cell death. Oncogene 27:1618–1628PubMedCrossRef
10.
go back to reference Baxley KO, Erdman LK, Henry EB, Roof BJ (1984) Alopecia: effect on cancer patients’ body image. Cancer Nurs 7:499–503PubMedCrossRef Baxley KO, Erdman LK, Henry EB, Roof BJ (1984) Alopecia: effect on cancer patients’ body image. Cancer Nurs 7:499–503PubMedCrossRef
11.
go back to reference Bhattacharya RK, Francis AR, Shetty TK (1987) Modifying role of dietary factors on the mutagenicity of aflatoxin B1: in vitro effect of vitamins. Mutat Res 188:121–128PubMedCrossRef Bhattacharya RK, Francis AR, Shetty TK (1987) Modifying role of dietary factors on the mutagenicity of aflatoxin B1: in vitro effect of vitamins. Mutat Res 188:121–128PubMedCrossRef
12.
go back to reference Blumm RH, Carter SK (1974) Adriamycin: a new anticancer drug with significant clinical activity. Ann Int Med 80:249–259 Blumm RH, Carter SK (1974) Adriamycin: a new anticancer drug with significant clinical activity. Ann Int Med 80:249–259
13.
go back to reference Borutaite V, Brown GC (2003) Nitric oxide induces apoptosis via hydrogen peroxide, but necrosis via energy and thiol depletion. Free Radic Biol Med 35:1457–1468PubMedCrossRef Borutaite V, Brown GC (2003) Nitric oxide induces apoptosis via hydrogen peroxide, but necrosis via energy and thiol depletion. Free Radic Biol Med 35:1457–1468PubMedCrossRef
14.
go back to reference Botchkarev VA (2003) Molecular mechanisms of chemotherapy-induced hair loss. J Invest Dermatol Symp Proc 8:72–75CrossRef Botchkarev VA (2003) Molecular mechanisms of chemotherapy-induced hair loss. J Invest Dermatol Symp Proc 8:72–75CrossRef
15.
go back to reference Botchkarev VA, Komarova EA, Siebenhaar F, Botchkareva NV, Komarov PG, Maurer M, Gilchrest BA, Gudkov AV (2000) p53 is essential for chemotherapy-induced hair loss. Cancer Res 60:5002–5006PubMed Botchkarev VA, Komarova EA, Siebenhaar F, Botchkareva NV, Komarov PG, Maurer M, Gilchrest BA, Gudkov AV (2000) p53 is essential for chemotherapy-induced hair loss. Cancer Res 60:5002–5006PubMed
16.
go back to reference Brezinska-Wcislo L (2001) Evaluation of vitamin B6 and calcium pantothenate effectiveness on hair growth from clinical and trichographic aspects for treatment of diffuse alopecia in women. Wiad Lek 54:11–18 Brezinska-Wcislo L (2001) Evaluation of vitamin B6 and calcium pantothenate effectiveness on hair growth from clinical and trichographic aspects for treatment of diffuse alopecia in women. Wiad Lek 54:11–18
17.
go back to reference Cannistraro S, van de Vorst A (1977) Hydrogen-adduct radicals in thymidine 5′-monophosphate photosensitized by proflavin. Protection by sulfur compounds. Biochim Biophys Acta 474:173–179PubMedCrossRef Cannistraro S, van de Vorst A (1977) Hydrogen-adduct radicals in thymidine 5′-monophosphate photosensitized by proflavin. Protection by sulfur compounds. Biochim Biophys Acta 474:173–179PubMedCrossRef
18.
go back to reference Cece R, Cazzaniga S, Morelli D, Sfondrini L, Bignotto M, Ménard S, Colnaghi MI, Balsari A (1996) Apoptosis of hair follicle cells during doxorubicin-induced alopecia in rats. Lab Invest 75:601–609PubMed Cece R, Cazzaniga S, Morelli D, Sfondrini L, Bignotto M, Ménard S, Colnaghi MI, Balsari A (1996) Apoptosis of hair follicle cells during doxorubicin-induced alopecia in rats. Lab Invest 75:601–609PubMed
19.
go back to reference Chen E, Cleaver JE, Weber CA (1994) Trichothiodystrophy: clinical spectrum, central nervous system imaging, and biochemical characterization of two siblings. J Invest Dermatol 103(Suppl 5):154S–158SPubMedCrossRef Chen E, Cleaver JE, Weber CA (1994) Trichothiodystrophy: clinical spectrum, central nervous system imaging, and biochemical characterization of two siblings. J Invest Dermatol 103(Suppl 5):154S–158SPubMedCrossRef
20.
21.
go back to reference Chumnantana R, Yokochi N, Yagi T (2005) Vitamin B6 compounds prevent the death of yeast cells due to menadione, a reactive oxygen generator. Biochim Biophys Acta 1722:84–91PubMedCrossRef Chumnantana R, Yokochi N, Yagi T (2005) Vitamin B6 compounds prevent the death of yeast cells due to menadione, a reactive oxygen generator. Biochim Biophys Acta 1722:84–91PubMedCrossRef
22.
go back to reference Ciesla Z, Filutowicz M (1979) Azide mutagenesis in gram-negative bacteria: reversion of the mutagenic effect by l-cystine. Mutat Res 66:301–305PubMedCrossRef Ciesla Z, Filutowicz M (1979) Azide mutagenesis in gram-negative bacteria: reversion of the mutagenic effect by l-cystine. Mutat Res 66:301–305PubMedCrossRef
23.
go back to reference Coburn SP, Slominski A, Mahuren JD, Wortsman J, Hessle L, Millan JL (2003) Cutaneous metabolism of vitamin B-6. J Invest Dermatol 120:292–300PubMedCrossRef Coburn SP, Slominski A, Mahuren JD, Wortsman J, Hessle L, Millan JL (2003) Cutaneous metabolism of vitamin B-6. J Invest Dermatol 120:292–300PubMedCrossRef
24.
go back to reference D’Agostini F, Bagnasco M, Giunciuglio D, Albini A, De Flora S (1998) Inhibition by oral n-acetylcysteine of doxorubicin-induced clastogenicity and alopecia, and prevention of primary tumors and lung micrometastases in mice. Int J Oncol 13:217–224PubMed D’Agostini F, Bagnasco M, Giunciuglio D, Albini A, De Flora S (1998) Inhibition by oral n-acetylcysteine of doxorubicin-induced clastogenicity and alopecia, and prevention of primary tumors and lung micrometastases in mice. Int J Oncol 13:217–224PubMed
25.
go back to reference D’Agostini F, Fiallo P, Pennisi TM, De Flora S (2007) Chemoprevention of smoke-induced alopecia in mice by oral administration of l-cystine and vitamin B6. J Dermatol Sci 46:189–198PubMedCrossRef D’Agostini F, Fiallo P, Pennisi TM, De Flora S (2007) Chemoprevention of smoke-induced alopecia in mice by oral administration of l-cystine and vitamin B6. J Dermatol Sci 46:189–198PubMedCrossRef
26.
go back to reference Dantchev D, Balercia G, Bourut C, Anjo A, Maral R, Mathé G (1984) Comparative microscopic study of cardiotoxicity and skin toxicity of anthracycline analogs. Biomed Pharmacother 38:322–328PubMed Dantchev D, Balercia G, Bourut C, Anjo A, Maral R, Mathé G (1984) Comparative microscopic study of cardiotoxicity and skin toxicity of anthracycline analogs. Biomed Pharmacother 38:322–328PubMed
27.
go back to reference Davis RH, Elzubeir EA, Craston JS (1988) Nutritional and biochemical factors influencing the biological effects of cyanide. Ciba Found Symp 140:219–231PubMed Davis RH, Elzubeir EA, Craston JS (1988) Nutritional and biochemical factors influencing the biological effects of cyanide. Ciba Found Symp 140:219–231PubMed
28.
go back to reference Davis ST, Benson BG, Bramson HN, Chapman DE, Dickerson SH, Chapman DE, Dickerson SH, Dold KM, Eberwein DJ, Edelstein M, Frye SV, Gampe RT Jr, Griffin RJ, Harris PA, Hassell AM, Holmes WD, Hunter RN, Knick VB, Lackey K, Lovejoy B, Luzzio MJ, Murray D, Parker P, Rocque WJ, Shewchuk L, Veal JM, Walker DH, Kuyper LF (2001) Prevention of chemotherapy-induced alopecia in rats by CDK inhibitors. Science 291:134–137PubMedCrossRef Davis ST, Benson BG, Bramson HN, Chapman DE, Dickerson SH, Chapman DE, Dickerson SH, Dold KM, Eberwein DJ, Edelstein M, Frye SV, Gampe RT Jr, Griffin RJ, Harris PA, Hassell AM, Holmes WD, Hunter RN, Knick VB, Lackey K, Lovejoy B, Luzzio MJ, Murray D, Parker P, Rocque WJ, Shewchuk L, Veal JM, Walker DH, Kuyper LF (2001) Prevention of chemotherapy-induced alopecia in rats by CDK inhibitors. Science 291:134–137PubMedCrossRef
29.
go back to reference Edenharder R, Worf-Wandelburg A, Decker M, Platt KL (1999) Antimutagenic effects and possible mechanisms of action of vitamins and related compounds against genotoxic heterocyclic amines from cooked food. Mutat Res 444:235–248PubMedCrossRef Edenharder R, Worf-Wandelburg A, Decker M, Platt KL (1999) Antimutagenic effects and possible mechanisms of action of vitamins and related compounds against genotoxic heterocyclic amines from cooked food. Mutat Res 444:235–248PubMedCrossRef
30.
go back to reference Endo N, Nishiyama K, Otsuka A, Kanouchi H, Taga M, Oka T (2006) Antioxidant activity of vitamin B6 delays homocysteine-induced atherosclerosis in rats. Br J Nutr 95:1088–1093PubMedCrossRef Endo N, Nishiyama K, Otsuka A, Kanouchi H, Taga M, Oka T (2006) Antioxidant activity of vitamin B6 delays homocysteine-induced atherosclerosis in rats. Br J Nutr 95:1088–1093PubMedCrossRef
31.
go back to reference Endo N, Nishiyama K, Okabe M, Matsumoto M, Kanouchi H, Oka T (2007) Vitamin B6 suppresses apoptosis of NM-1 bovine endothelial cells induced by homocysteine and copper. Biochim Biophys Acta 1770:571–577PubMedCrossRef Endo N, Nishiyama K, Okabe M, Matsumoto M, Kanouchi H, Oka T (2007) Vitamin B6 suppresses apoptosis of NM-1 bovine endothelial cells induced by homocysteine and copper. Biochim Biophys Acta 1770:571–577PubMedCrossRef
32.
go back to reference Friesen C, Kiess Y, Debatin KM (2004) A critical role of glutathione in determining apoptosis sensitivity and resistance in leukemia cells. Cell Death Differ Suppl 1:S73–S85CrossRef Friesen C, Kiess Y, Debatin KM (2004) A critical role of glutathione in determining apoptosis sensitivity and resistance in leukemia cells. Cell Death Differ Suppl 1:S73–S85CrossRef
33.
go back to reference Go Y-M, Jones DP (2008) Redox compartmentalization in eukaryotic cells. Biochim Biophys Acta 1780:1273–1290PubMedCrossRef Go Y-M, Jones DP (2008) Redox compartmentalization in eukaryotic cells. Biochim Biophys Acta 1780:1273–1290PubMedCrossRef
34.
go back to reference Green PS, Leeuwenburgh C (2002) Mitochondrial dysfunction is an early indicator of doxorubicin-induced apoptosis. Biochim Biophys Acta 1588:94–101PubMedCrossRef Green PS, Leeuwenburgh C (2002) Mitochondrial dysfunction is an early indicator of doxorubicin-induced apoptosis. Biochim Biophys Acta 1588:94–101PubMedCrossRef
35.
go back to reference Gross P, Runne E, Wilson JW (1948) Studies on the effect of thallium poisoning of the rat. The influence of cystine and methionine on alopecia and survival periods. J Invest Dermatol 10:119–134PubMed Gross P, Runne E, Wilson JW (1948) Studies on the effect of thallium poisoning of the rat. The influence of cystine and methionine on alopecia and survival periods. J Invest Dermatol 10:119–134PubMed
36.
go back to reference Gummer CL, Dawber RP, Price VH (1984) Trichothiodystrophy: an electron-histochemical study of the hair shaft. Br J Dermatol 110:439–449PubMedCrossRef Gummer CL, Dawber RP, Price VH (1984) Trichothiodystrophy: an electron-histochemical study of the hair shaft. Br J Dermatol 110:439–449PubMedCrossRef
37.
go back to reference György P (1964) History of vitamin B-6. Introductory remarks. Vitam Horm 22:361–365CrossRef György P (1964) History of vitamin B-6. Introductory remarks. Vitam Horm 22:361–365CrossRef
38.
go back to reference Harrison S, Sinclair R (2003) Optimal management of hair loss (alopecia) in children. Am J Clin Dermatol 4:757–770PubMedCrossRef Harrison S, Sinclair R (2003) Optimal management of hair loss (alopecia) in children. Am J Clin Dermatol 4:757–770PubMedCrossRef
39.
go back to reference Helmreich EJ (1992) How pyridoxal-5′-phosphate could function in glycogen phosphorylase catalysis. Biofactors 3:159–172PubMed Helmreich EJ (1992) How pyridoxal-5′-phosphate could function in glycogen phosphorylase catalysis. Biofactors 3:159–172PubMed
40.
go back to reference Hertel H, Gollnick H, Matthies C, Baumann I, Orfanos CE (1989) Low dosage retinol and l-cystine combination improve alopecia of the diffuse type following long-term oral administration. Hautarzt 40:490–498PubMed Hertel H, Gollnick H, Matthies C, Baumann I, Orfanos CE (1989) Low dosage retinol and l-cystine combination improve alopecia of the diffuse type following long-term oral administration. Hautarzt 40:490–498PubMed
41.
go back to reference Hess WC (1949) The rates of absorption and the formation of liver glycogen by methionine, cystine, and cysteine. J Biol Chem 181:23–30PubMed Hess WC (1949) The rates of absorption and the formation of liver glycogen by methionine, cystine, and cysteine. J Biol Chem 181:23–30PubMed
42.
go back to reference Holmes DIR, Zachary I (2005) The vascular endothelial growth factor (VEGF) family: angiogenic factors in health and disease. Genome Biol 6:209PubMedCrossRef Holmes DIR, Zachary I (2005) The vascular endothelial growth factor (VEGF) family: angiogenic factors in health and disease. Genome Biol 6:209PubMedCrossRef
43.
go back to reference Hrelia S, Fiorentini D, Maraldi T, Angeloni C, Bordoni A, Biagi PL, Hakim G (2002) Doxorubicin induces early lipid peroxidation associated with changes in glucose transport in cultured cardiomyocytes. Biochim Biophys Acta 1567:150–156PubMedCrossRef Hrelia S, Fiorentini D, Maraldi T, Angeloni C, Bordoni A, Biagi PL, Hakim G (2002) Doxorubicin induces early lipid peroxidation associated with changes in glucose transport in cultured cardiomyocytes. Biochim Biophys Acta 1567:150–156PubMedCrossRef
44.
go back to reference Hu S, Zhao H, Al-Humadi NH, Yin XJ, Ma JK (2006) Silica-induced apoptosis in alveolar macrophages: evidence of in vivo thiol depletion and the activation of mitochondrial pathway. J Toxicol Environ Health 69:1261–1284CrossRef Hu S, Zhao H, Al-Humadi NH, Yin XJ, Ma JK (2006) Silica-induced apoptosis in alveolar macrophages: evidence of in vivo thiol depletion and the activation of mitochondrial pathway. J Toxicol Environ Health 69:1261–1284CrossRef
45.
go back to reference Ishaque A, Al-Rubeai M (2002) Role of vitamins in determining apoptosis and extent of suppression by bcl-2 during hybridoma cell culture. Apoptosis 7:231–239PubMedCrossRef Ishaque A, Al-Rubeai M (2002) Role of vitamins in determining apoptosis and extent of suppression by bcl-2 during hybridoma cell culture. Apoptosis 7:231–239PubMedCrossRef
46.
go back to reference Jiang S, Moriarty-Craige SE, Orr M, Cai J, Sternberg P, Jones DP (2005) Oxidant-induced apoptosis in human retinal pigment epithelial cells: dependence on extracellular redox state. Invest Ophtalmol Vis Sci 46:1054–1061CrossRef Jiang S, Moriarty-Craige SE, Orr M, Cai J, Sternberg P, Jones DP (2005) Oxidant-induced apoptosis in human retinal pigment epithelial cells: dependence on extracellular redox state. Invest Ophtalmol Vis Sci 46:1054–1061CrossRef
47.
go back to reference Jimenez JJ, Roberts SM, Mejia J, Mauro LM, Munson JW, Elgart GW, Connelly EA, Chen Q, Zou J, Goldenberg C, Voellmy R (2008) Prevention of chemotherapy-induced alopecia in rodent models. Cell Stress Chaperones 13:31–38PubMedCrossRef Jimenez JJ, Roberts SM, Mejia J, Mauro LM, Munson JW, Elgart GW, Connelly EA, Chen Q, Zou J, Goldenberg C, Voellmy R (2008) Prevention of chemotherapy-induced alopecia in rodent models. Cell Stress Chaperones 13:31–38PubMedCrossRef
48.
go back to reference Jonas CR, Ziegler TR, Gu LH, Jones DP (2002) Extracellular thiol/disulfide redox state affects proliferation rate in a human colon carcinoma cell line. Free Radic Biol Med 33:1499–1506PubMedCrossRef Jonas CR, Ziegler TR, Gu LH, Jones DP (2002) Extracellular thiol/disulfide redox state affects proliferation rate in a human colon carcinoma cell line. Free Radic Biol Med 33:1499–1506PubMedCrossRef
49.
go back to reference Jones DP, Go Y-M, Anderson CL, Ziegler TR, Kinkade JM, Kirlin WG (2004) Cysteine/cystine couple is a newly recognized node in the circuitry for biologic redox signaling and control. FASEB J 18:1246–1248PubMed Jones DP, Go Y-M, Anderson CL, Ziegler TR, Kinkade JM, Kirlin WG (2004) Cysteine/cystine couple is a newly recognized node in the circuitry for biologic redox signaling and control. FASEB J 18:1246–1248PubMed
50.
go back to reference Kalivendi SV, Kotamraju S, Zhao H, Joseph J, Kalyanaraman B (2001) Doxorubicin-induced apoptosis is associated with increased transcription of endothelial nitric-oxide synthase. J Biol Chem 276:47266–47276PubMedCrossRef Kalivendi SV, Kotamraju S, Zhao H, Joseph J, Kalyanaraman B (2001) Doxorubicin-induced apoptosis is associated with increased transcription of endothelial nitric-oxide synthase. J Biol Chem 276:47266–47276PubMedCrossRef
51.
go back to reference Kannan K, Jain SK (2004) Effect of vitamin B6 on oxygen radicals, mitochondrial membrane potential, and lipid peroxidation in H2O2-treated U397 monocytes. Free Radic Biol Med 36:423–428PubMedCrossRef Kannan K, Jain SK (2004) Effect of vitamin B6 on oxygen radicals, mitochondrial membrane potential, and lipid peroxidation in H2O2-treated U397 monocytes. Free Radic Biol Med 36:423–428PubMedCrossRef
52.
go back to reference Kim EJ, Lim KM, Kim KY, Bae ON, Noh JY, Chung SM, Shin S, Yun YP, Chung JH (2009) Doxorubicin-induced platelet cytotoxicity: a new contributory factor for doxorubicin-mediated thrombocytopenia. J Thromb Haemost 7:1172–1183PubMedCrossRef Kim EJ, Lim KM, Kim KY, Bae ON, Noh JY, Chung SM, Shin S, Yun YP, Chung JH (2009) Doxorubicin-induced platelet cytotoxicity: a new contributory factor for doxorubicin-mediated thrombocytopenia. J Thromb Haemost 7:1172–1183PubMedCrossRef
53.
go back to reference Kojima S, Miyazaki Y, Honda T, Kiyozumi M, Shimada H, Funakoshi T (1992) Effect of l-cystine on toxicity of paraquat in mice. Toxicol Lett 60:75–82PubMedCrossRef Kojima S, Miyazaki Y, Honda T, Kiyozumi M, Shimada H, Funakoshi T (1992) Effect of l-cystine on toxicity of paraquat in mice. Toxicol Lett 60:75–82PubMedCrossRef
54.
go back to reference Komatsu S, Yanaka N, Matsubara K, Kato N (2003) Antitumor effect of vitamin B6 and its mechanisms. Biochim Biophys Acta 1647:127–130PubMedCrossRef Komatsu S, Yanaka N, Matsubara K, Kato N (2003) Antitumor effect of vitamin B6 and its mechanisms. Biochim Biophys Acta 1647:127–130PubMedCrossRef
55.
go back to reference Kovár J, Stýbrová H, Truksa J, Spĕváková K, Valenta T (2002) Apoptosis induction in lymphoma cells: thiol deprivation versus thiol excess. Folia Biol (Praha) 48:58–68 Kovár J, Stýbrová H, Truksa J, Spĕváková K, Valenta T (2002) Apoptosis induction in lymphoma cells: thiol deprivation versus thiol excess. Folia Biol (Praha) 48:58–68
56.
go back to reference Kuwashima Y (1996) Cytomorphology of murine B16 melanoma in vivo after treatment with cyclophosphamide: evidence for ‘oncotic’ cell death. Anticancer Res 16:2997–3000PubMed Kuwashima Y (1996) Cytomorphology of murine B16 melanoma in vivo after treatment with cyclophosphamide: evidence for ‘oncotic’ cell death. Anticancer Res 16:2997–3000PubMed
57.
go back to reference Kuznetsov AV, Margreiter R, Amberger A, Saks V, Grimm M (2011) Changes in mitochondrial redox state, membrane potential and calcium precede mitochondrial dysfunction in doxorubicin-induced cell death. Biochim Biophys Acta 1813:1144–1152PubMedCrossRef Kuznetsov AV, Margreiter R, Amberger A, Saks V, Grimm M (2011) Changes in mitochondrial redox state, membrane potential and calcium precede mitochondrial dysfunction in doxorubicin-induced cell death. Biochim Biophys Acta 1813:1144–1152PubMedCrossRef
58.
go back to reference L’Ecuyer TJ, Allebban Z, Thomas R, van der Heide R (2004) Glutathione-S-transferase overexpression protects against anthracycline-induced H9C2 cell death. Am J Physiol Heart Circ Physiol 286:H2057–H2064PubMedCrossRef L’Ecuyer TJ, Allebban Z, Thomas R, van der Heide R (2004) Glutathione-S-transferase overexpression protects against anthracycline-induced H9C2 cell death. Am J Physiol Heart Circ Physiol 286:H2057–H2064PubMedCrossRef
59.
go back to reference Lengg N, Heidecker B, Seifert B, Trüeb RM (2007) Dietary supplement increases anagen hair rate in women with telogen effluvium: results of a double-blind placebo-controlled trial. Therapy 4:59–65CrossRef Lengg N, Heidecker B, Seifert B, Trüeb RM (2007) Dietary supplement increases anagen hair rate in women with telogen effluvium: results of a double-blind placebo-controlled trial. Therapy 4:59–65CrossRef
60.
go back to reference Li L, Mignone J, Yang M, Matic M, Penman S, Enikolopov G, Hoffman RM (2003) Nestin expression in hair follicle sheath progenitor cells. PNAS USA 100:9958–9961PubMedCrossRef Li L, Mignone J, Yang M, Matic M, Penman S, Enikolopov G, Hoffman RM (2003) Nestin expression in hair follicle sheath progenitor cells. PNAS USA 100:9958–9961PubMedCrossRef
61.
go back to reference Lind DS, Kontaridis MI, Edwards PD et al (1997) Nitric oxide contributes to adriamycin’s antitumor effect. J Surg Res 69:283–287PubMedCrossRef Lind DS, Kontaridis MI, Edwards PD et al (1997) Nitric oxide contributes to adriamycin’s antitumor effect. J Surg Res 69:283–287PubMedCrossRef
62.
go back to reference Mahfouz MM, Kummerow FA (2004) Vitamin C or vitamin B6 supplementation prevent the oxidative stress and decrease of prostacyclin generation in homocysteinemic rats. Int J Biochem Cell Biol 36:1919–1932PubMedCrossRef Mahfouz MM, Kummerow FA (2004) Vitamin C or vitamin B6 supplementation prevent the oxidative stress and decrease of prostacyclin generation in homocysteinemic rats. Int J Biochem Cell Biol 36:1919–1932PubMedCrossRef
63.
go back to reference Mahfouz MM, Zhou SQ, Kummerow FA (2009) Vitamin B6 compounds are capable of reducing the superoxide radical and lipid peroxide levels induced by H2O2 in vascular endothelial cells in culture. Int J Vitam Nutr Res 79:218–219PubMedCrossRef Mahfouz MM, Zhou SQ, Kummerow FA (2009) Vitamin B6 compounds are capable of reducing the superoxide radical and lipid peroxide levels induced by H2O2 in vascular endothelial cells in culture. Int J Vitam Nutr Res 79:218–219PubMedCrossRef
64.
go back to reference Mailloux A, Grenet K, Bruneel A, Bénéteau-Burnat B, Vaubourdolle M, Baudin B (2001) Anticancer drugs induce necrosis of human endothelial cells involving both oncosis and apoptosis. Eur J Cell Biol 80:442–449PubMedCrossRef Mailloux A, Grenet K, Bruneel A, Bénéteau-Burnat B, Vaubourdolle M, Baudin B (2001) Anticancer drugs induce necrosis of human endothelial cells involving both oncosis and apoptosis. Eur J Cell Biol 80:442–449PubMedCrossRef
65.
go back to reference Malkinson FD, Geng L, Hanson WR (1993) Prostaglandins protect against murine hair injury produced by ionizing radiation or doxorubicin. J Invest Dermatol 101:135S–137SPubMedCrossRef Malkinson FD, Geng L, Hanson WR (1993) Prostaglandins protect against murine hair injury produced by ionizing radiation or doxorubicin. J Invest Dermatol 101:135S–137SPubMedCrossRef
66.
go back to reference Matsubara K, Komatsu S, Oka T, Kato N (2003) Vitamin B6-mediated suppression of colon tumorigenesis, cell proliferation, and angiogenesis. J Nutr Biochem 14:246–250PubMedCrossRef Matsubara K, Komatsu S, Oka T, Kato N (2003) Vitamin B6-mediated suppression of colon tumorigenesis, cell proliferation, and angiogenesis. J Nutr Biochem 14:246–250PubMedCrossRef
67.
go back to reference McGarvey EL, Baum LD, Pinkerton RC, Rogers LM (2001) Psychological sequelae and alopecia among women with cancer. Cancer Pract 9:283–289PubMedCrossRef McGarvey EL, Baum LD, Pinkerton RC, Rogers LM (2001) Psychological sequelae and alopecia among women with cancer. Cancer Pract 9:283–289PubMedCrossRef
68.
go back to reference Mehta R, Dedina L, O’Brien PJ (2011) Rescuing hepatocytes from iron-catalyzed oxidative stress using vitamins B1 and B6. Toxicol In Vitro 25:1114–1122PubMedCrossRef Mehta R, Dedina L, O’Brien PJ (2011) Rescuing hepatocytes from iron-catalyzed oxidative stress using vitamins B1 and B6. Toxicol In Vitro 25:1114–1122PubMedCrossRef
69.
go back to reference Mooney S, Leuendorf J-E, Hendrickson C, Hellmann H (2009) Vitamin B6: a long known compound of surprising complexity. Molecules 14:329–351PubMedCrossRef Mooney S, Leuendorf J-E, Hendrickson C, Hellmann H (2009) Vitamin B6: a long known compound of surprising complexity. Molecules 14:329–351PubMedCrossRef
70.
go back to reference Munstedt K, Manthey S, Sachsse S, Vahrson H (1997) Changes in self-concept and body image during alopecia induced cancer chemotherapy. Support Care Cancer 5:139–143PubMedCrossRef Munstedt K, Manthey S, Sachsse S, Vahrson H (1997) Changes in self-concept and body image during alopecia induced cancer chemotherapy. Support Care Cancer 5:139–143PubMedCrossRef
71.
go back to reference Narisawa S, Wennberg C, Millàn JL (2001) Abnormal vitamin B6 metabolism in alkaline phosphatase knock-out mice causes multiple abnormalities, but not the impaired bone mineralization. J Pathol 193:125–133PubMedCrossRef Narisawa S, Wennberg C, Millàn JL (2001) Abnormal vitamin B6 metabolism in alkaline phosphatase knock-out mice causes multiple abnormalities, but not the impaired bone mineralization. J Pathol 193:125–133PubMedCrossRef
72.
go back to reference Petri H, Pierchalla P, Tronnier H (1990) The efficacy of drug therapy in structural lesions of the hair and in diffuse effluvium—comparative double blind study. Schweiz Rundsch Med Prax 79:1457–1462PubMed Petri H, Pierchalla P, Tronnier H (1990) The efficacy of drug therapy in structural lesions of the hair and in diffuse effluvium—comparative double blind study. Schweiz Rundsch Med Prax 79:1457–1462PubMed
73.
go back to reference Porter RM, Jahoda CA, Lunny DP, Henderson G, Ross J, McLean WH, Whittock N, Wilson NJ, Reichelt J, Magin T, Lane E (2002) Defolliculated (D−): a dominant mouse mutation leading to poor sebaceous gland differentiation and total elimination of pelage follicles. J Invest Dermatol 119:32–37PubMedCrossRef Porter RM, Jahoda CA, Lunny DP, Henderson G, Ross J, McLean WH, Whittock N, Wilson NJ, Reichelt J, Magin T, Lane E (2002) Defolliculated (D): a dominant mouse mutation leading to poor sebaceous gland differentiation and total elimination of pelage follicles. J Invest Dermatol 119:32–37PubMedCrossRef
74.
go back to reference Prasad R, Lakshmi AV, Bamji MS (1983) Impaired collagen maturity in vitamins B-2 and B-6 deficiency. Probable molecular basis of skin lesions. Biochem Med 30:333–341PubMedCrossRef Prasad R, Lakshmi AV, Bamji MS (1983) Impaired collagen maturity in vitamins B-2 and B-6 deficiency. Probable molecular basis of skin lesions. Biochem Med 30:333–341PubMedCrossRef
75.
go back to reference Sadot E, Geiger B, Oren M, Ben-Ze’ev A (2001) Downregulation of beta-catenin by activated p53. Mol Cell Biol 21:6768–6781PubMedCrossRef Sadot E, Geiger B, Oren M, Ben-Ze’ev A (2001) Downregulation of beta-catenin by activated p53. Mol Cell Biol 21:6768–6781PubMedCrossRef
76.
go back to reference Selleri S, Arnaboldi F, Vizzotto L, Balsari A, Rumio C (2004) Epithelium–mesenchyme compartment interaction and oncosis on chemotherapy-induced hair damage. Lab Investig 84:1404–1417PubMedCrossRef Selleri S, Arnaboldi F, Vizzotto L, Balsari A, Rumio C (2004) Epithelium–mesenchyme compartment interaction and oncosis on chemotherapy-induced hair damage. Lab Investig 84:1404–1417PubMedCrossRef
77.
go back to reference Selleri S, Seltmann H, Gariboldi S, Shirai YF, Balsari A, Zouboulis CC, Rumio C (2006) Doxorubicin-induced alopecia is associated with sebaceous gland degeneration. J Invest Dermatol 126:711–720PubMedCrossRef Selleri S, Seltmann H, Gariboldi S, Shirai YF, Balsari A, Zouboulis CC, Rumio C (2006) Doxorubicin-induced alopecia is associated with sebaceous gland degeneration. J Invest Dermatol 126:711–720PubMedCrossRef
78.
go back to reference Shetty TK, Francis AR, Bhattacharya RK (1989) Modifying role of dietary factors on the mutagenicity of aflatoxin B1: in vitro effect of sulphur-containing amino acids. Mutat Res 222:403–407PubMedCrossRef Shetty TK, Francis AR, Bhattacharya RK (1989) Modifying role of dietary factors on the mutagenicity of aflatoxin B1: in vitro effect of sulphur-containing amino acids. Mutat Res 222:403–407PubMedCrossRef
79.
go back to reference Shimoi K, Akaiwa E, Mori N, Sano M, Nakamura Y, Tomita I (1992) Bio-antimutagenic activities of vitamin B6 in E. coli and mouse peripheral blood cells. Mutat Res 266:205–213PubMedCrossRef Shimoi K, Akaiwa E, Mori N, Sano M, Nakamura Y, Tomita I (1992) Bio-antimutagenic activities of vitamin B6 in E. coli and mouse peripheral blood cells. Mutat Res 266:205–213PubMedCrossRef
80.
go back to reference Skladanowski A, Konopa J (1994) Relevance of interstrand DNA crosslinking induced by anthracyclines for their biological activity. Biochem Pharmacol 47:2279–2287PubMedCrossRef Skladanowski A, Konopa J (1994) Relevance of interstrand DNA crosslinking induced by anthracyclines for their biological activity. Biochem Pharmacol 47:2279–2287PubMedCrossRef
81.
go back to reference Spiegel D, Giese-Davis J (2003) Depression and cancer: mechanisms and disease progression. Biol Psychiatry 54:269–282PubMedCrossRef Spiegel D, Giese-Davis J (2003) Depression and cancer: mechanisms and disease progression. Biol Psychiatry 54:269–282PubMedCrossRef
82.
go back to reference Stenn KS (2001) Insights from the asebia mouse: a molecular sebaceous gland defect leading to cicatricial alopecia. J Cutan Pathol 28:445–447PubMedCrossRef Stenn KS (2001) Insights from the asebia mouse: a molecular sebaceous gland defect leading to cicatricial alopecia. J Cutan Pathol 28:445–447PubMedCrossRef
83.
go back to reference Story MD, Meyn RE (1999) Modulation of apoptosis and enhancement of chemosensitivity by decreasing cellular thiols in a mouse B-cell lymphoma cell line that overexpress bcl-2. Cancer Chemother Pharmacol 44:362–366PubMedCrossRef Story MD, Meyn RE (1999) Modulation of apoptosis and enhancement of chemosensitivity by decreasing cellular thiols in a mouse B-cell lymphoma cell line that overexpress bcl-2. Cancer Chemother Pharmacol 44:362–366PubMedCrossRef
84.
go back to reference Szabò L, Matkovitcs B, Barabàs K, Oroszlàn G (1986) Effects of various thiols on paraquat toxicity. Comp Biochem Physiol C 83:149–153PubMedCrossRef Szabò L, Matkovitcs B, Barabàs K, Oroszlàn G (1986) Effects of various thiols on paraquat toxicity. Comp Biochem Physiol C 83:149–153PubMedCrossRef
85.
go back to reference Tanaka R (1997) Induction of a sister-chromatid exchange by nitrogen oxides and its prevention by SOD. J Toxicol Sci 22:199–205PubMedCrossRef Tanaka R (1997) Induction of a sister-chromatid exchange by nitrogen oxides and its prevention by SOD. J Toxicol Sci 22:199–205PubMedCrossRef
86.
go back to reference Thotala D, Chetyrkin S, Hudson B, Hallahan D, Voziyan P, Yazlovitskaya E (2009) Pyridoxamine protects intestinal epithelium from ionizing radiation-induced apoptosis. Free Radic Biol Med 47:779–785PubMedCrossRef Thotala D, Chetyrkin S, Hudson B, Hallahan D, Voziyan P, Yazlovitskaya E (2009) Pyridoxamine protects intestinal epithelium from ionizing radiation-induced apoptosis. Free Radic Biol Med 47:779–785PubMedCrossRef
87.
go back to reference Troyano A, Fernàndez C, Sancho P, de Blas E, Aller P (2001) Effect of glutathione depletion on antitumor drug toxicity (apoptosis and necrosis) in U-397 human promonocytic cells. The role of intracellular oxidation. J Biol Chem 276:47107–47115PubMedCrossRef Troyano A, Fernàndez C, Sancho P, de Blas E, Aller P (2001) Effect of glutathione depletion on antitumor drug toxicity (apoptosis and necrosis) in U-397 human promonocytic cells. The role of intracellular oxidation. J Biol Chem 276:47107–47115PubMedCrossRef
88.
89.
go back to reference Tsang WP, Chau SP, Kong SK, Fung KP, Kwok TT (2003) Reactive oxygen species mediate doxorubicin induced p53-independent apoptosis. Life Sci 73:2047–2058PubMedCrossRef Tsang WP, Chau SP, Kong SK, Fung KP, Kwok TT (2003) Reactive oxygen species mediate doxorubicin induced p53-independent apoptosis. Life Sci 73:2047–2058PubMedCrossRef
90.
go back to reference Uchugonova A, Duong J, Zhang N, König K, Hoffman RM (2011) The bulge area is the origin of nestin-expressing pluripotent stem cells of the hair follicle. J Cell Biochem 112:2046–2050PubMedCrossRef Uchugonova A, Duong J, Zhang N, König K, Hoffman RM (2011) The bulge area is the origin of nestin-expressing pluripotent stem cells of the hair follicle. J Cell Biochem 112:2046–2050PubMedCrossRef
91.
go back to reference Vialkowitsch B (1962) The treatment of seborrheic disease picture and falling hair with vitamin B6. Med Welt 22:1260–1262PubMed Vialkowitsch B (1962) The treatment of seborrheic disease picture and falling hair with vitamin B6. Med Welt 22:1260–1262PubMed
92.
go back to reference Vitt UA, Hsu SY, Hsueh AJ (2001) Evolution and classification of cystine knot-containing hormones and related extracellular signaling molecules. Mol Endocrinol 15:681–694PubMedCrossRef Vitt UA, Hsu SY, Hsueh AJ (2001) Evolution and classification of cystine knot-containing hormones and related extracellular signaling molecules. Mol Endocrinol 15:681–694PubMedCrossRef
93.
go back to reference Wagner L, Gorely M (1979) Body image and patients experiencing alopecia as a result of cancer chemotherapy. Cancer Nurs 2:365–369PubMedCrossRef Wagner L, Gorely M (1979) Body image and patients experiencing alopecia as a result of cancer chemotherapy. Cancer Nurs 2:365–369PubMedCrossRef
94.
go back to reference Wang J, Lu Z, Au JLS (2006) Protection against chemotherapy-induced alopecia. Pharm Res 23:2505–2514PubMedCrossRef Wang J, Lu Z, Au JLS (2006) Protection against chemotherapy-induced alopecia. Pharm Res 23:2505–2514PubMedCrossRef
95.
go back to reference Wen YF, Zhao JQ, Bhadauria M, Nirala SK (2010) Pyridoxine mitigates cadmium induced hepatic cytotoxicity and oxidative stress. Environ Toxicol Pharmacol 30:169–174PubMedCrossRef Wen YF, Zhao JQ, Bhadauria M, Nirala SK (2010) Pyridoxine mitigates cadmium induced hepatic cytotoxicity and oxidative stress. Environ Toxicol Pharmacol 30:169–174PubMedCrossRef
96.
go back to reference Williams R, Philpott MP, Kealey T (1993) Metabolism of freshly isolated human hair follicles capable of hair elongation: a glutaminolytic, aerobic glycolytic tissue. J Invest Dermatol 100:834–840PubMedCrossRef Williams R, Philpott MP, Kealey T (1993) Metabolism of freshly isolated human hair follicles capable of hair elongation: a glutaminolytic, aerobic glycolytic tissue. J Invest Dermatol 100:834–840PubMedCrossRef
97.
go back to reference Wu G, Fang Y-Z, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implication for health. J Nutr 134:489–492PubMed Wu G, Fang Y-Z, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implication for health. J Nutr 134:489–492PubMed
98.
go back to reference Wu HY, Jan TR (2010) Cannabidiol hydroxyquinone-induced apoptosis of splenocytes is mediated predominantly by thiol depletion. Toxicol Lett 195:68–74PubMedCrossRef Wu HY, Jan TR (2010) Cannabidiol hydroxyquinone-induced apoptosis of splenocytes is mediated predominantly by thiol depletion. Toxicol Lett 195:68–74PubMedCrossRef
99.
go back to reference Yang CF, Shen HM, Ong CN (2000) Intracellular thiol depletion causes mitochondrial permeability transition in ebselen-induced apoptosis. Arch Biochem Biophys 380:319–330PubMedCrossRef Yang CF, Shen HM, Ong CN (2000) Intracellular thiol depletion causes mitochondrial permeability transition in ebselen-induced apoptosis. Arch Biochem Biophys 380:319–330PubMedCrossRef
100.
go back to reference Zahn H, Gattner HG (1997) Hair sulfur amino acid analysis. EXS 78:239–258PubMed Zahn H, Gattner HG (1997) Hair sulfur amino acid analysis. EXS 78:239–258PubMed
101.
go back to reference Zeman SM, Phillips DR, Crothers DM (1998) Characterization of covalent adriamycin-DNA adducts. PNAS USA 95:11561–11565PubMedCrossRef Zeman SM, Phillips DR, Crothers DM (1998) Characterization of covalent adriamycin-DNA adducts. PNAS USA 95:11561–11565PubMedCrossRef
Metadata
Title
Chemoprevention of doxorubicin-induced alopecia in mice by dietary administration of l-cystine and vitamin B6
Authors
Francesco D’Agostini
Paolo Fiallo
Massimo Ghio
Silvio De Flora
Publication date
01-01-2013
Publisher
Springer-Verlag
Published in
Archives of Dermatological Research / Issue 1/2013
Print ISSN: 0340-3696
Electronic ISSN: 1432-069X
DOI
https://doi.org/10.1007/s00403-012-1253-1

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