Loss of epidermal hypoxia-inducible factor-1α accelerates epidermal aging and affects re-epithelialization in human and mouse

Journal of Cell Science

Volumn 124, Issue 24, 2011, Pages 4172-4183

  Rezvani, Hamid Reza ^a,b   Ali, Nsrein ^a,b   Serrano Sanchez, Martin ^a,b   Dubus, Pierre ^b   Varon, Christine ^c   Ged, Cécile ^a,b   Pain, Catherine ^a,b   Cario André, Muriel ^a,b,d   Seneschal, Julien ^a,b,d   Taïeb, Alain ^a,b,d   de Verneuil, Hubert ^a,b   Mazurier, Frédéric ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c U853 ^*  (France)

^d HÔPITAL SAINT ANDRÉ   (France)

Author keywords

Aging; Dermatitis; Epidermis; Hypoxia inducible factor; Skin; Wound healing

Indexed keywords

ALPHA6 INTEGRIN; BETA1 INTEGRIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LAMININ;

ARTICLE; BASEMENT MEMBRANE; CELL AGING; CELL GROWTH; CONTROLLED STUDY; EPIDERMAL AGING; EPIDERMIS; EPITHELIZATION; HOMEOSTASIS; HUMAN; KERATINOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PRURITUS; SKIN; SKIN ATROPHY;

AGING; ANIMALS; APOPTOSIS; CELL ADHESION MOLECULES; CELL CYCLE CHECKPOINTS; DOWN-REGULATION; EPIDERMIS; GENE KNOCKOUT TECHNIQUES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTEGRINS; KERATINOCYTES; MICE; PHENOTYPE; SKIN; WOUND HEALING;

MUS;

EID: 84856905397     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.082370     Document Type: Article

References (78)

1. Adams, J. C. and Watt, F. M.(1990). Changes in keratinocyte adhesion during terminal differentiation: reduction in fibronectin binding precedes alpha 5 beta 1 integrin loss from the cell surface. Cell 63, 425-435.
2. Bedogni, B., Welford, S. M., Cassarino, D. S., Nickoloff, B. J., Giaccia, A. J. and Powell, M. B.(2005). The hypoxic microenvironment of the skin contributes to Aktmediated melanocyte transformation. Cancer Cell 8, 443-454.
3. Berra, E., Ginouves, A. and Pouyssegur, J.(2006). The hypoxia-inducible-factor hydroxylases bring fresh air into hypoxia signalling. EMBO Rep. 7, 41-45.
4. Biswas, S., Roy, S., Banerjee, J., Hussain, S. R., Khanna, S., Meenakshisundaram, G., Kuppusamy, P., Friedman, A. and Sen, C. K.(2010). Hypoxia inducible microRNA 210 attenuates keratinocyte proliferation and impairs closure in a murine model of ischemic wounds. Proc. Natl. Acad. Sci. USA 107, 6976-6981.
5. Bosch-Marce, M., Okuyama, H., Wesley, J. B., Sarkar, K., Kimura, H., Liu, Y. V., Zhang, H., Strazza, M., Rey, S., Savino, L. et al.(2007). Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia. Circ. Res. 101, 1310-1318.
6. Botusan, I. R., Sunkari, V. G., Savu, O., Catrina, A. I., Grunler, J., Lindberg, S., Pereira, T., Yla-Herttuala, S., Poellinger, L., Brismar, K. et al.(2008). Stabilization of HIF-1αlpha is critical to improve wound healing in diabetic mice. Proc. Natl. Acad. Sci. USA 105, 19426-19431.
7. Boutin, A. T., Weidemann, A., Fu, Z., Mesropian, L., Gradin, K., Jamora, C., Wiesener, M., Eckardt, K. U., Koch, C. J., Ellies, L. G. et al.(2008). Epidermal sensing of oxygen is essential for systemic hypoxic response. Cell 133, 223-234.
8. Brakebusch, C., Grose, R., Quondamatteo, F., Ramirez, A., Jorcano, J. L., Pirro, A., Svensson, M., Herken, R., Sasaki, T., Timpl, R. et al.(2000). Skin and hair follicle integrity is crucially dependent on beta 1 integrin expression on keratinocytes. EMBO J. 19, 3990-4003.
9. Burgeson, R. E. and Christiano, A. M.(1997). The dermal-epidermal junction. Curr. Opin. Cell Biol. 9, 651-658.
10. Ceradini, D. J., Kulkarni, A. R., Callaghan, M. J., Tepper, O. M., Bastidas, N., Kleinman, M. E., Capla, J. M., Galiano, R. D., Levine, J. P. and Gurtner, G. C.(2004). Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 10, 858-864.
11. Chang, E. I., Loh, S. A., Ceradini, D. J., Chang, E. I., Lin, S. E., Bastidas, N., Aarabi, S., Chan, D. A., Freedman, M. L., Giaccia, A. J. et al.(2007). Age decreases endothelial progenitor cell recruitment through decreases in hypoxiainducible factor 1alpha stabilization during ischemia. Circulation 116, 2818-2829.
12. Cho, Y. S., Bae, J. M., Chun, Y. S., Chung, J. H., Jeon, Y. K., Kim, I. S., Kim, M. S. and Park, J. W.(2008). HIF-1αlpha controls keratinocyte proliferation by upregulating p21(WAF1/Cip1). Biochim. Biophys. Acta. 1783, 323-333.
13. Cramer, T., Yamanishi, Y., Clausen, B. E., Forster, I., Pawlinski, R., Mackman, N., Haase, V. H., Jaenisch, R., Corr, M., Nizet, V. et al.(2003). HIF-1αlpha is essential for myeloid cell-mediated inflammation. Cell 112, 645-657.
14. Distler, O., Distler, J. H., Scheid, A., Acker, T., Hirth, A., Rethage, J., Michel, B. A., Gay, R. E., Muller-Ladner, U., Matucci-Cerinic, M. et al.(2004). Uncontrolled expression of vascular endothelial growth factor and its receptors leads to insufficient skin angiogenesis in patients with systemic sclerosis. Circ. Res. 95, 109-116.
15. Elson, D. A., Ryan, H. E., Snow, J. W., Johnson, R. and Arbeit, J. M.(2000). Coordinate up-regulation of hypoxia inducible factor (HIF)-1alpha and HIF-1 target genes during multi-stage epidermal carcinogenesis and wound healing. Cancer Res. 60, 6189-6195.
16. Elson, D. A., Thurston, G., Huang, L. E., Ginzinger, D. G., McDonald, D. M., Johnson, R. S. and Arbeit, J. M.(2001). Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1alpha. Genes Dev. 15, 2520-2532.
17. Evans, N. T. and Naylor, P. F.(1967). The oxygen tension gradient across human epidermis. Respir. Physiol. 3, 38-42.
18. Fine, J. D., Eady, R. A., Bauer, E. A., Bauer, J. W., Bruckner-Tuderman, L., Heagerty, A., Hintner, H., Hovnanian, A., Jonkman, M. F., Leigh, I. et al.(2008). The classification of inherited epidermolysis bullosa (EB): Report of the Third International Consensus Meeting on Diagnosis and Classification of EB. J. Am. Acad. Dermatol. 58, 931-950.
19. Fitsialos, G., Bourget, I., Augier, S., Ginouves, A., Rezzonico, R., Odorisio, T., Cianfarani, F., Virolle, T., Pouyssegur, J., Meneguzzi, G. et al.(2008). HIF1 transcription factor regulates laminin-332 expression and keratinocyte migration. J. Cell Sci. 121, 2992-3001.
20. Fluhr, J. W., Darlenski, R., Taieb, A., Hachem, J. P., Baudouin, C., Msika, P., De Belilovsky, C. and Berardesca, E.(2010). Functional skin adaptation in infancy -almost complete but not fully competent. Exp. Dermatol. 19, 483-492.
21. Forsythe, J. A., Jiang, B. H., Iyer, N. V., Agani, F., Leung, S. W., Koos, R. D. and Semenza, G. L.(1996). Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16, 4604-4613.
22. Frank, S. and Kampfer, H.(2003). Excisional wound healing. An experimental approach. Methods Mol. Med. 78, 3-15.
23. Gagnoux-Palacios, L., Vailly, J., Durand-Clement, M., Wagner, E., Ortonne, J. P. and Meneguzzi, G.(1996). Functional Re-expression of laminin-5 in laminingamma2-deficient human keratinocytes modifies cell morphology, motility, and adhesion. J Biol. Chem. 271, 18437-18444.
24. Grose, R., Hutter, C., Bloch, W., Thorey, I., Watt, F. M., Fassler, R., Brakebusch, C. andWerner, S.(2002). A crucial role of beta 1 integrins for keratinocyte migration in vitro and during cutaneous wound repair. Development 129, 2303-2315.
25. Huang, L. E., Gu, J., Schau, M. and Bunn, H. F.(1998). Regulation of hypoxiainducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 95, 7987-7992.
26. Indra, A. K., Warot, X., Brocard, J., Bornert, J. M., Xiao, J. H., Chambon, P. and Metzger, D.(1999). Temporally-controlled site-specific mutagenesis in the basal layer of the epidermis: comparison of the recombinase activity of the tamoxifeninducible Cre-ER(T) and Cre-ER(T2) recombinases. Nucleic Acids Res. 27, 4324-4327.
27. Ivan, M., Kondo, K., Yang, H., Kim, W., Valiando, J., Ohh, M., Salic, A., Asara, J. M., Lane, W. S. and Kaelin, W. G., Jr.(2001). HIFalpha targeted for VHLmediated destruction by proline hydroxylation: implications for O2 sensing. Science 292, 464-468.
28. Kallio, P. J., Wilson, W. J., O'Brien, S., Makino, Y. and Poellinger, L.(1999). Regulation of the hypoxia-inducible transcription factor 1alpha by the ubiquitinproteasome pathway. J Biol. Chem. 274, 6519-6525.
29. Kelly, B. D., Hackett, S. F., Hirota, K., Oshima, Y., Cai, Z., Berg-Dixon, S., Rowan, A., Yan, Z., Campochiaro, P. A. and Semenza, G. L.(2003). Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1. Circ. Res. 93, 1074-1081.
30. Keely, S., Glover, L. E., MacManus, C. F., Campbell, E. L., Scully, M. M., Furuta, G. T. and Colgan, S. P.(2009). Selective induction of integrin beta1 by hypoxiainducible factor: implications for wound healing. FASEB J. 23, 1338-1346.
31. Kietzmann, T. and Gorlach, A.(2005). Reactive oxygen species in the control of hypoxia-inducible factor-mediated gene expression. Semin. Cell. Dev. Biol. 16, 474-486.
32. Kim, K. S., Rajagopal, V., Gonsalves, C., Johnson, C. and Kalra, V. K.(2006). A novel role of hypoxia-inducible factor in cobalt chloride- and hypoxia-mediated expression of IL-8 chemokine in human endothelial cells. J. Immunol. 177, 7211-7224.
33. Li, M., Chiba, H., Warot, X., Messaddeq, N., Gerard, C., Chambon, P. and Metzger, D.(2001). RXR-alpha ablation in skin keratinocytes results in alopecia and epidermal alterations. Development 128, 675-688.
34. Li, W., Li, Y., Guan, S., Fan, J., Cheng, C. F., Bright, A. M., Chinn, C., Chen, M., and Woodley, D. T.(2007). Extracellular heat shock protein-90alpha: linking hypoxia to skin cell motility and wound healing. EMBO J. 26, 1221-1233.
35. Liu, L., Marti, G. P., Wei, X., Zhang, X., Zhang, H., Liu, Y. V., Nastai, M., Semenza, G. L. and Harmon, J. W.(2008). Age-dependent impairment of HIF-1αlpha expression in diabetic mice: Correction with electroporation-facilitated gene therapy increases wound healing, angiogenesis, and circulating angiogenic cells. J. Cell. Physiol. 217, 319-327.
36. Loh, S. A., Chang, E. I., Galvez, M. G., Thangarajah, H., El-ftesi, S., Vial, I. N., Lin, D. A. and Gurtner, G. C.(2009). SDF-1 alpha expression during wound healing in the aged is HIF dependent. Plast. Reconstr. Surg. 123, 65S-75S.
37. Lopez-Rovira, T., Silva-Vargas, V. and Watt, F. M.(2005). Different consequences of beta1 integrin deletion in neonatal and adult mouse epidermis reveal a contextdependent role of integrins in regulating proliferation, differentiation, and intercellular communication. J. Invest. Dermatol. 125, 1215-1227.
38. Mace, K. A., Yu, D. H., Paydar, K. Z., Boudreau, N. and Young, D. M.(2007). Sustained expression of Hif-1alpha in the diabetic environment promotes angiogenesis and cutaneous wound repair. Wound Repair Regen. 15, 636-645.
39. Margadant, C., Raymond, K., Kreft, M., Sachs, N., Janssen, H. and Sonnenberg, A.(2009). Integrin alpha3beta1 inhibits directional migration and wound re-epithelialization in the skin. J. Cell Sci. 122, 278-288.
40. Maxwell, P. H.(2004). HIF-19s relationship to oxygen: simple yet sophisticated. Cell Cycle 3, 156-159.
41. Maxwell, P. H., Pugh, C. W. and Ratcliffe, P. J.(2001). The pVHL-hIF-1 system. A key mediator of oxygen homeostasis. Adv. Exp. Med. Biol. 502, 365-376.
42. Metzen, E. and Ratcliffe, P. J.(2004). HIF hydroxylation and cellular oxygen sensing. Biol. Chem 385, 223-230.
43. Michaylira, C. Z. and Nakagawa, H.(2006). Hypoxic microenvironment as a cradle for melanoma development and progression. Cancer Biol. Ther. 5, 476-479.
44. Morice-Picard, F., Cario-Andre, M., Rezvani, H., Lacombe, D., Sarasin, A. and Taieb, A.(2009). New clinico-genetic classification of trichothiodystrophy. Am. J. Med. Genet. A 149A, 2020-2030.
45. Nakano, A., Chao, S. C., Pulkkinen, L., Murrell, D., Bruckner-Tuderman, L., Pfendner, E. and Uitto, J.(2002). Laminin 5 mutations in junctional epidermolysis bullosa: molecular basis of Herlitz vs. non-Herlitz phenotypes. Hum. Genet. 110, 41-51.
46. Ninikoski, J., Heughan, C. and Hunt, T. K.(1972). Oxygen tensions in human wounds. J. Surg. Res. 12, 77-82.
47. O'Toole, E. A., Marinkovich, M. P., Hoeffler, W. K., Furthmayr, H. and Woodley, D. T.(1997). Laminin-5 inhibits human keratinocyte migration. Exp. Cell Res. 233, 330-339.
48. Oyoshi, M. K., Murphy, G. F. and Geha, R. S.(2009). Filaggrin-deficient mice exhibit TH17-dominated skin inflammation and permissiveness to epicutaneous sensitization with protein antigen. J. Allergy Clin. Immunol. 124, 485-493.
49. Piwko-Czuchra, A., Koegel, H., Meyer, H., Bauer, M., Werner, S., Brakebusch, C. and Fassler, R.(2009). Beta1 integrin-mediated adhesion signalling is essential for epidermal progenitor cell expansion. PLoS One 4, e5488.
50. Pouyssegur, J., Dayan, F. and Mazure, N. M.(2006). Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441, 437-443.
51. Proksch, E., Brandner, J. M. and Jensen, J. M.(2008). The skin: an indispensable barrier. Exp. Dermatol. 17, 1063-1072.
52. Rezvani, H. R., Mazurier, F., Cario-Andre, M., Pain, C., Ged, C., Taieb, A. and de Verneuil, H.(2006). Protective effects of catalase overexpression on UVB-induced apoptosis in normal human keratinocytes. J. Biol. Chem. 281, 17999-18007.
53. Rezvani, H. R., Cario-Andre, M., Pain, C., Ged, C., deVerneuil, H. and Taieb, A.(2007a). Protection of normal human reconstructed epidermis from UV by catalase overexpression. Cancer Gene Therapy 14, 174-186.
54. Rezvani, H. R., Dedieu, S., North, S., Belloc, F., Rossignol, R., Letellier, T., de Verneuil, H., Taieb, A. and Mazurier, F.(2007b). Hypoxia-inducible factor-1alpha, a key factor in the keratinocyte response to UVB exposure. J. Biol. Chem. 282, 16413-16422.
55. Rezvani, H. R., Ged, C., Bouadjar, B., de Verneuil, H. and Taieb, A.(2008). Catalase overexpression reduces UVB-induced apoptosis in a human xeroderma pigmentosum reconstructed epidermis. Cancer Gene Therapy 15, 241-251.
56. Rezvani, H. R., Mahfouf, W., Ali, N., Chemin, C., Ged, C., Kim, A. L., de Verneuil, H., Taieb, A., Bickers, D. R. and Mazurier, F.(2010a). Hypoxia-inducible factor-1alpha regulates the expression of nucleotide excision repair proteins in keratinocytes. Nucleic Acids Res. 38, 797-809.
57. Rezvani, H. R., Mazurier, F., Morice-Picard, F., Jouary, T., Cario-André, M., Ged, C., de Verneuil, H. and Tai{dotless}̈eb, A.(2010b). Xeroderma pigmentosum: clues to understanding cancer initiation. Dermatologica sinica 28, 93-101.
58. Rezvani, H. R., Ali, N., Nissen, L. J., Harfouche, G., de Verneuil, H., Tai{dotless}̈eb, A., Mazurier, F.(2011a). HIF-1αlpha in epidermis: oxygen sensing, cutaneous angiogenesis, cancer, and non cancer disorders. J. Invest. Dermatol. 31, 1793-1805.
59. Rezvani, H. R., Kim, A. L., Rossignol, R., Ali, N., Daly, M., Mahfouf, W., Bellance, N., Taieb, A., de Verneuil, H., Mazurier, F. et al.(2011b). XPC silencing in normal human keratinocytes triggers metabolic alterations that drive the formation of squamous cell carcinomas. J. Clin. Invest. 121, 195-211.
60. Rezvani, H. R., Rossignol, R., Ali, N., Benard, G., Tang, X., Yang, H. S., Jouary, T., de Verneuil, H., Taieb, A., Kim, A. L. et al.(2011c). XPC silencing in normal human keratinocytes triggers metabolic alterations through NOX-1 activationmediated reactive oxygen species. Biochim. Biophys. Acta. 1807, 609-619.
61. Rosenberger, C., Solovan, C., Rosenberger, A. D., Jinping, L., Treudler, R., Frei, U., Eckardt, K. U. and Brown, L. F.(2007). Upregulation of hypoxia-inducible factors in normal and psoriatic skin. J. Invest. Dermatol. 127, 2445-2452.
62. Rousselle, P., Lunstrum, G. P., Keene, D. R. and Burgeson, R. E.(1991). Kalinin: an epithelium-specific basement membrane adhesion molecule that is a component of anchoring filaments. J. Cell Biol. 114, 567-576.
63. Ryan, M. C., Christiano, A. M., Engvall, E., Wewer, U. M., Miner, J. H., Sanes, J. R. and Burgeson, R. E.(1996). The functions of laminins: lessons from in vivo studies. Matrix Biol. 15, 369-381.
64. Ryan, H. E., Lo, J. and Johnson, R. S.(1998). HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J. 17, 3005-3015.
65. Salceda, S. and Caro, J.(1997). Hypoxia-inducible factor 1alpha (HIF-1αlpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem. 272, 22642-22647.
66. Semenza, G. L.(2003). Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732.
67. 2-regulated gene expression: transcriptional control of cardiorespiratory physiology by HIF-1. J. Appl. Physiol. 96, 1173-1177.
68. Semenza, G. L. and Wang, G. L.(1992). A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell. Biol. 12, 5447-5454.
69. Sen, C. K., Khanna, S., Babior, B. M., Hunt, T. K., Ellison, E. C. and Roy, S.(2002). Oxidant-induced vascular endothelial growth factor expression in human keratinocytes and cutaneous wound healing. J. Biol. Chem. 277, 33284-33290.
70. Stewart, F. A., Denekamp, J. and Randhawa, V. S.(1982). Skin sensitization by misonidazole: a demonstration of uniform mild hypoxia. Br. J. Cancer 45, 869-877.
71. Taney, K.(2008). Secondary cleft palate repair. J. Vet. Dent. 25, 150-153.
72. Vailly, J., Gagnoux-Palacios, L., Dell'Ambra, E., Romero, C., Pinola, M., Zambruno, G., De Luca, M., Ortonne, J. P. and Meneguzzi, G.(1998). Corrective gene transfer of keratinocytes from patients with junctional epidermolysis bullosa restores assembly of hemidesmosomes in reconstructed epithelia. Gene Ther. 5, 1322-1332.
73. Varghese, M. C., Balin, A. K., Carter, D. M. and Caldwell, D.(1986). Local environment of chronic wounds under synthetic dressings. Arch. Dermatol. 122, 52-57.
74. 2 tension. Proc. Natl. Acad. Sci. USA 92, 5510-5514.
75. Watt, F. M.(2002). Role of integrins in regulating epidermal adhesion, growth and differentiation. EMBO J. 21, 3919-3926.
76. 2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB J. 16, 1151-1162.
77. Woodley, D. T., Fan, J., Cheng, C. F., Li, Y., Chen, M., Bu, G. and Li, W.(2009). Participation of the lipoprotein receptor LRP1 in hypoxia-HSP90alpha autocrine signaling to promote keratinocyte migration. J. Cell Sci. 122, 1495-1498.
78. Zhang, X., Liu, L., Wei, X., Tan, Y. S., Tong, L., Chang, R., Ghanamah, M. S., Reinblatt, M., Marti, G. P., Harmon, J.W. et al.(2010). Impaired angiogenesis and mobilization of circulating angiogenic cells in HIF-1αlpha heterozygous-null mice after burn wounding. Wound Repair Regen. 18, 193-201.