Hypoxia inducible microRNA 210 attenuates keratinocyte proliferation and impairs closure in a murine model of ischemic wounds

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 15, 2010, Pages 6976-6981

  Biswas, Sabyasachi ^a   Roy, Sashwati ^a   Banerjee, Jaideep ^a   Hussain, Syed Rehan A ^a   Khanna, Savita ^a   Meenakshisundaram, Guruguhan ^a   Kuppusamy, Periannan ^a   Friedman, Avner ^b   Sen, Chandan K ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Skin; Tissue repair; Wound healing

Indexed keywords

HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; KI 67 ANTIGEN; MICRORNA; REGULATOR PROTEIN; TRANSCRIPTION FACTOR E2F3;

ADENOVIRUS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD FLOW; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ELECTRON SPIN RESONANCE; EPITHELIZATION; HUMAN; HUMAN CELL; HYPOXIA; ISCHEMIA; KERATINOCYTE; MACROPHAGE; MOLECULAR IMAGING; MOLECULAR MIMICRY; MOUSE; NONHUMAN; OXIMETRY; OXYGEN SATURATION; PEDICLED SKIN FLAP; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE OXYGENATION; UPREGULATION; WOUND CLOSURE; WOUND HEALING IMPAIRMENT;

ANIMALS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; ISCHEMIA; KERATINOCYTES; KI-67 ANTIGEN; LASER-DOPPLER FLOWMETRY; MACROPHAGES; MICE; MICE, INBRED C57BL; MICRORNAS; WOUND HEALING;

MURINAE;

EID: 77951043486     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1001653107     Document Type: Article

References (42)

1. Sen CK, et al. (2009) Human skin wounds: a major and snowballing threat to public health and the economy. Wound Repair Regen 17:763-771.
2. Sen CK (2009) Wound healing essentials: let there be oxygen. Wound Repair Regen 17:1-18.
3. Powell RJ, et al. (2008) Results of a double-blind, placebo-controlled study to assess the safety of intramuscular injection of hepatocyte growth factor plasmid to improve limb perfusion in patients with critical limb ischemia. Circulation 118:58-65.
4. Roy S, et al. (2009) Characterization of a preclinical model of chronic ischemic wound. Physiol Genomics 37:211-224.
5. Kerrigan CL, Daniel RK (1984) Skin flap research: a candid view. Ann Plast Surg 13:383-387.
6. Kerrigan CL, Daniel RK (1982) Critical ischemia time and the failing skin flap. Plast Reconstr Surg 69:986-989. (Pubitemid 12074683)
7. Khan F, Newton DJ (2003) Laser Doppler imaging in the investigation of lower limb wounds. Int J Low Extrem Wounds 2:74-86.
8. Khaodhiar L, et al. (2007) The use of medical hyperspectral technology to evaluate microcirculatory changes in diabetic foot ulcers and to predict clinical outcomes. Diabetes Care 30:903-910. (Pubitemid 46556585)
9. Greenman RL, et al. (2005) Early changes in the skin microcirculation and muscle metabolism of the diabetic foot. Lancet 366:1711-1717.
10. Mathieu D, Mani R (2007) A review of the clinical significance of tissue hypoxia measurements in lower extremity wound management. Int J Low Extrem Wounds 6:273-283. (Pubitemid 350131918)
11. Franzeck UK, Talke P, Bernstein EF, Golbranson FL, Fronek A (1982) Transcutaneous PO2 measurements in health and peripheral arterial occlusive disease. Surgery 91:156-163. (Pubitemid 12168582)
12. Harward TR, Volny J, Golbranson F, Bernstein EF, Fronek A (1985) Oxygen inhalation - induced transcutaneous PO2 changes as a predictor of amputation level. J Vasc Surg 2:220-227. (Pubitemid 15054148)
13. Roy S, Khanna S, Rink C, Biswas S, Sen CK (2008) Characterization of the acute temporal changes in excisional murine cutaneous wound inflammation by screening of the wound-edge transcriptome. Physiol Genomics 34:162-184.
14. Scortegagna M, Martin RJ, Kladney RD, Neumann RG, Arbeit JM (2009) Hypoxiainducible factor-1alpha suppresses squamous carcinogenic progression and epithelial-mesenchymal transition. Cancer Res 69:2638-2646.
15. Sen CK, Gordillo GM, Khanna S, Roy S (2009) Micromanaging vascular biology: tiny microRNAs play big band. J Vasc Res 46:527-540.
16. Gammell P (2007) MicroRNAs: recently discovered key regulators of proliferation and apoptosis in animal cells : Identification of miRNAs regulating growth and survival. Cytotechnology 53:55-63.
17. Giannakakis A, et al. (2008) miR-210 links hypoxia with cell cycle regulation and is deleted in human epithelial ovarian cancer. Cancer Biol Ther 7:255-264. (Pubitemid 351590433)
18. Sen CK, et al. (2002) Oxidant-induced vascular endothelial growth factor expression in human keratinocytes and cutaneous wound healing. J Biol Chem 277:33284-33290. (Pubitemid 34984849)
19. Quirinia A (2000) Ischemic wound healing and possible treatments. Drugs Today (Barc) 36:41-53.
20. Slovut DP, Sullivan TM (2008) Critical limb ischemia: medical and surgical management. Vasc Med 13:281-291.
21. Fujihara Y, et al. (2008) Controlled delivery of bFGF to recipient bed enhances the vascularization and viability of an ischemic skin flap. Wound Repair Regen 16:125-131.
22. Mittermayr R, et al. (2008) Sustained (rh)VEGF(165) release from a sprayed fibrin biomatrix induces angiogenesis, up-regulation of endogenous VEGF-R2, and reduces ischemic flap necrosis. Wound Repair Regen 16:542-550. (Pubitemid 352000310)
23. Tanaka R, et al. (2008) The effects of flap ischemia on normal and diabetic progenitor cell function. Plast Reconstr Surg 121:1929-1942.
24. Leor J, et al. (2006) Ex vivo activated human macrophages improve healing, remodeling, and function of the infarcted heart. Circulation 114 (1, Suppl):I94-I100. (Pubitemid 44297135)
25. Orenstein A, et al. (2005) Treatment of deep sternal wound infections post-open heart surgery by application of activated macrophage suspension. Wound Repair Regen 13:237-242. (Pubitemid 40848015)
26. Food and Drug Administration (2006), ed. Services, U.S.D.o.H.a.H. (Food and Drug Administration, Regulatory Guidance.) http://www.fda.gov/downloads/ Drugs/GuidanceComplianceRegulatoryInformation/Guidances/ucm071324.pdf.
27. Kopal C, Deveci M, Oztürk S, Sengezer M (2007) Effects of topical glutathione treatment in rat ischemic wound model. Ann Plast Surg 58:449-455. (Pubitemid 46569074)
28. Liechty KW, et al. (1999) Adenoviral-mediated overexpression of platelet-derived growth factor-B corrects ischemic impaired wound healing. J Invest Dermatol 113:375-383.
29. Sun W, et al. (2007) Collagen membranes loaded with collagen-binding human PDGFBB accelerate wound healing in a rabbit dermal ischemic ulcer model. Growth Factors 25:309-318. (Pubitemid 351194029)
30. Chang WY, Andrews J, Carter DE, Dagnino L (2006) Differentiation and injury-repair signals modulate the interaction of E2F and pRB proteins with novel target genes in keratinocytes. Cell Cycle 5:1872-1879. (Pubitemid 44435333)
31. Jones SJ, Dicker AJ, Dahler AL, Saunders NA (1997) E2F as a regulator of keratinocyte proliferation: implications for skin tumor development. J Invest Dermatol 109:187-193.
32. Chang WY, Bryce DM, D'Souza SJ, Dagnino L (2004) The DP-1 transcription factor is required for keratinocyte growth and epidermal stratification. J Biol Chem 279:51343-51353. (Pubitemid 40017881)
33. Huang X, et al. (2009) Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell 35:856-867.
34. Chan SY, et al. (2009) MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2. Cell Metab 10:273-284.
35. Ojha N, et al. (2008) Assessment of wound-site redox environment and the significance of Rac2 in cutaneous healing. Free Radic Biol Med 44:682-691.
36. Roy S, Khanna S, Nallu K, Hunt TK, Sen CK (2006) Dermal wound healing is subject to redox control. Mol Ther 13:211-220. (Pubitemid 41763500)
37. Meenakshisundaram G, et al. (2009) Oxygen sensitivity and biocompatibility of an implantable paramagnetic probe for repeated measurements of tissue oxygenation. Biomed Microdevices 11:817-826.
38. Ratan RR, et al. (2008) Small molecule activation of adaptive gene expression: tilorone or its analogs are novel potent activators of hypoxia inducible factor-1 that provide prophylaxis against stroke and spinal cord injury. Ann N Y Acad Sci 1147:383-394.
39. Underwood RA, Gibran NS, Muffley LA, Usui ML, Olerud JE (2001) Color subtractive-computer-assisted image analysis for quantification of cutaneous nerves in a diabetic mouse model. J Histochem Cytochem 49:1285-1291.
40. Roy S, et al. (2007) Transcriptome-wide analysis of blood vessels laser captured from human skin and chronic wound-edge tissue. Proc Natl Acad Sci USA 104:14472-14477. (Pubitemid 350003285)
41. Aminova LR, et al. (2005) Prosurvival and prodeath effects of hypoxia-inducible factor-1alpha stabilization in a murine hippocampal cell line. J Biol Chem 280:3996-4003.
42. Shilo S, Roy S, Khanna S, Sen CK (2008) Evidence for the involvement of miRNA in redox regulated angiogenic response of human microvascular endothelial cells. Arterioscler Thromb Vasc Biol 28:471-477.