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Lactate stimulates angiogenesis and accelerates the healing of superficial and ischemic wounds in mice.

Onglets principaux

Porporato, Paolo [UCL] Payen, Valéry [UCL] De Saedeleer, Christophe [UCL] Préat, Véronique [UCL] Thissen, Jean-Paul [UCL] Feron, Olivier [UCL] Sonveaux, Pierre [UCL]

Wounds notoriously accumulate lactate as a consequence of both anaerobic and aerobic glycolysis following microcirculation disruption, immune activation, and increased cell proliferation. Several pieces of evidence suggest that lactate actively participates in the healing process through the activation of several molecular pathways that collectively promote angiogenesis. Lactate indeed stimulates endothelial cell migration and tube formation in vitro, as well as the recruitment of circulating vascular progenitor cells and vascular morphogenesis in vivo. In this study, we examined whether the pro-angiogenic potential of lactate may be exploited therapeutically to accelerate wound healing. We show that lactate delivered from a Matrigel matrix improves reperfusion and opposes muscular atrophy in ischemic hindlimb wounds in mice. Both responses involve lactate-induced reparative angiogenesis. Using microdialysis and enzymatic measurements, we found that, contrary to poly-L-lactide (PLA), a subcutaneous implant of poly-D,L-lactide-co-glycolide (PLGA) allows sustained local and systemic lactate release. PLGA promoted angiogenesis and accelerated the closure of excisional skin wounds in different mouse strains. This polymer is FDA-approved for other applications, emphasizing the possibility of exploiting PLGA therapeutically to improve wound healing.

Type de document Article de périodique (Journal article) – Article de recherche
Type d'accès Accès mixte
Année de publication 2012
Langue Anglais
Information sur le périodique "Angiogenesis" - Vol. 15, p. 581-592 (2012)
Peer reviewed oui
Editeur Springer Netherlands ((Netherlands) Dordrecht)
issn 0969-6970
Statut de la publication Publié
Affiliations UCL - SSS/IREC/FATH - Pôle de Pharmacologie et thérapeutique
UCL - SSS/LDRI - Louvain Drug Research Institute
UCL - SSS/IREC/EDIN - Pôle d'endocrinologie, diabète et nutrition
UCL - (SLuc) Service d'endocrinologie et de nutrition
Liens
  1. Trabold Odilo, Wagner Silvia, Wicke Corinna, Scheuenstuhl Heinz, Hussain M. Zamirul, Rosen Noah, Seremetiev Alan, Becker Horst D., Hunt Thomas K., Lactate and oxygen constitute a fundamental regulatory mechanism in wound healing, 10.1046/j.1524-475x.2003.11621.x
  2. HALESTRAP Andrew P., PRICE Nigel T., The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation, 10.1042/0264-6021:3430281
  3. Halestrap Andrew P., Meredith David, The SLC16 gene family?from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond, 10.1007/s00424-003-1067-2
  4. Schreml S., Szeimies R.M., Prantl L., Karrer S., Landthaler M., Babilas P., Oxygen in acute and chronic wound healing : Oxygen in wound healing, 10.1111/j.1365-2133.2010.09804.x
  5. Vander Heiden M. G., Cantley L. C., Thompson C. B., Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation, 10.1126/science.1160809
  6. Hunt Thomas K., Conolly W.Bruce, Aronson Samuel B., Goldstein Phillip, Anaerobic metabolism and wound healing: An hypothesis for the initiation and cessation of collagen synthesis in wounds, 10.1016/0002-9610(78)90061-2
  7. Ghani Q. Perveen, Wagner Silvia, Hussain M. Zamirul, Role of ADP-ribosylation in wound repair. The contributions of Thomas K. Hunt, MD, 10.1046/j.1524-475x.2003.11608.x
  8. Gladden L. B., Lactate metabolism: a new paradigm for the third millennium : Lactate metabolism, 10.1113/jphysiol.2003.058701
  9. GREEN HOWARD, GOLDBERG BURTON, Collagen and Cell Protein Synthesis by an Established Mammalian Fibroblast Line, 10.1038/204347a0
  10. Hussain MZ, Ghani QP, Hunt TK (1989) Inhibition of prolyl hydroxylase by poly(ADP-ribose) and phosphoribosyl-AMP. Possible role of ADP-ribosylation in intracellular prolyl hydroxylase regulation. J Biol Chem 264:7850–7855
  11. Constant James S, Feng John J, Zabel David D, Yuan Hui, Suh David Y, Scheuenstuhl Heinz, Hunt Thomas K, Hussain M. Zamirul, Lactate elicits vascular endothelial growth factor from macrophages: a possible alternative to hypoxia, 10.1111/j.1524-475x.2000.00353.x
  12. Xiong Ming, Elson Genie, Legarda Diana, Leibovich Samuel Joseph, Production of Vascular Endothelial Growth Factor by Murine Macrophages, 10.1016/s0002-9440(10)65601-5
  13. Kumar V.B. Sameer, Viji R.I., Kiran M.S., Sudhakaran P.R., Endothelial cell response to lactate: Implication of PAR modification of VEGF, 10.1002/jcp.20955
  14. Vegran F., Boidot R., Michiels C., Sonveaux P., Feron O., Lactate Influx through the Endothelial Cell Monocarboxylate Transporter MCT1 Supports an NF- B/IL-8 Pathway that Drives Tumor Angiogenesis, 10.1158/0008-5472.can-10-2828
  15. Sonveaux Pierre, Copetti Tamara, De Saedeleer Christophe J., Végran Frédérique, Verrax Julien, Kennedy Kelly M., Moon Eui Jung, Dhup Suveera, Danhier Pierre, Frérart Françoise, Gallez Bernard, Ribeiro Anthony, Michiels Carine, Dewhirst Mark W., Feron Olivier, Targeting the Lactate Transporter MCT1 in Endothelial Cells Inhibits Lactate-Induced HIF-1 Activation and Tumor Angiogenesis, 10.1371/journal.pone.0033418
  16. Lu Huasheng, Forbes Robert A., Verma Ajay, Hypoxia-inducible Factor 1 Activation by Aerobic Glycolysis Implicates the Warburg Effect in Carcinogenesis, 10.1074/jbc.m202487200
  17. Lu Huasheng, Dalgard Clifton L., Mohyeldin Ahmed, McFate Thomas, Tait A. Sasha, Verma Ajay, Reversible Inactivation of HIF-1 Prolyl Hydroxylases Allows Cell Metabolism to Control Basal HIF-1, 10.1074/jbc.m508718200
  18. Li Fang, Sonveaux Pierre, Rabbani Zahid N., Liu Shanling, Yan Bin, Huang Qian, Vujaskovic Zeljko, Dewhirst Mark W., Li Chuan-Yuan, Regulation of HIF-1α Stability through S-Nitrosylation, 10.1016/j.molcel.2007.02.024
  19. Milovanova T. N., Bhopale V. M., Sorokina E. M., Moore J. S., Hunt T. K., Hauer-Jensen M., Velazquez O. C., Thom S. R., Lactate Stimulates Vasculogenic Stem Cells via the Thioredoxin System and Engages an Autocrine Activation Loop Involving Hypoxia-Inducible Factor 1, 10.1128/mcb.00795-08
  20. Murray Brenda, Wilson D.J., 10.1023/a:1016792319207
  21. Beckert Stefan, Farrahi Farshid, Aslam Rummana S., Scheuenstuhl Heinz, Königsrainer Alfred, Hussain M. Zamirul, Hunt Thomas K., Lactate stimulates endothelial cell migration : Lactate stimulates endothelial cell migration, 10.1111/j.1743-6109.2006.00127.x
  22. Burns P.A., Wilson D.J., 10.1023/a:1025862731653
  23. Hunt Thomas K., Aslam Rummana S., Beckert Stefan, Wagner Silvia, Ghani Q. Perveen, Hussain M. Zamirul, Roy Sashwati, Sen Chandan K., Aerobically Derived Lactate Stimulates Revascularization and Tissue RepairviaRedox Mechanisms, 10.1089/ars.2007.1674
  24. Couffinhal T, Silver M et al (1998) Mouse model of angiogenesis. Am J Pathol 152:1667–1679
  25. Sonveaux P., Caveolin-1 Expression Is Critical for Vascular Endothelial Growth Factor-Induced Ischemic Hindlimb Collateralization and Nitric Oxide-Mediated Angiogenesis, 10.1161/01.res.0000136344.27825.72
  26. Del Prete E., Lutz T.A., Scharrer E., Inhibition of glucose oxidation by α-cyano-4-hydroxycinnamic acid stimulates feeding in rats, 10.1016/j.physbeh.2003.10.007
  27. Sonveaux P, Vegran F et al (2008) Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest 118:3930–3942
  28. Hishiya Akinori, Iemura Shun-ichiro, Natsume Tohru, Takayama Shinichi, Ikeda Kyoji, Watanabe Ken, A novel ubiquitin-binding protein ZNF216 functioning in muscle atrophy, 10.1038/sj.emboj.7600945
  29. Dehoux Mischael, Van Beneden Ronald, Pasko Nevi, Lause Pascale, Verniers Josiane, Underwood Louis, Ketelslegers Jean-Marie, Thissen Jean-Paul, Role of the Insulin-Like Growth Factor I Decline in the Induction of Atrogin-1/MAFbx during Fasting and Diabetes, 10.1210/en.2004-0406
  30. Cao Y., Sonveaux P., Liu S., Zhao Y., Mi J., Clary B. M., Li C.-Y., Kontos C. D., Dewhirst M. W., Systemic Overexpression of Angiopoietin-2 Promotes Tumor Microvessel Regression and Inhibits Angiogenesis and Tumor Growth, 10.1158/0008-5472.can-06-4056
  31. Peters Thorsten, Sindrilaru Anca, Hinz Boris, Hinrichs Ralf, Menke André, Al-Azzeh Ezz Al Din, Holzwarth Katrin, Oreshkova Tsvetelina, Wang Honglin, Kess Daniel, Walzog Barbara, Sulyok Silke, Sunderkötter Cord, Friedrich Wilhelm, Wlaschek Meinhard, Krieg Thomas, Scharffetter-Kochanek Karin, Wound-healing defect of CD18−/− mice due to a decrease in TGF-β1 and myofibroblast differentiation, 10.1038/sj.emboj.7600809
  32. Gutierrez-Fernandez A., Inada M., Balbin M., Fueyo A., Pitiot A. S., Astudillo A., Hirose K., Hirata M., Shapiro S. D., Noel A., Werb Z., Krane S. M., Lopez-Otin C., Puente X. S., Increased inflammation delays wound healing in mice deficient in collagenase-2 (MMP-8), 10.1096/fj.06-7860com
  33. Sindrilaru A., Peters T., Schymeinsky J., Oreshkova T., Wang H., Gompf A., Mannella F., Wlaschek M., Sunderkotter C., Rudolph K. L., Walzog B., Bustelo X. R., Fischer K. D., Scharffetter-Kochanek K., Wound healing defect of Vav3-/- mice due to impaired  2-integrin-dependent macrophage phagocytosis of apoptotic neutrophils, 10.1182/blood-2008-07-166702
  34. Milch Hannah S., Schubert Shai Y., Hammond Stephen, Spiegel Jeffrey H., Enhancement of ischemic wound healing by inducement of local angiogenesis, 10.1002/lary.21068
  35. Mendel DB, Schreck RE et al (2000) The angiogenesis inhibitor SU5416 has long-lasting effects on vascular endothelial growth factor receptor phosphorylation and function. Clin Cancer Res 6:4848–4858
  36. Manning Fox JE, Meredith D, Halestrap AP (2000) Characterisation of human monocarboxylate transporter 4 substantiates its role in lactic acid efflux from skeletal muscle. J Physiol 529(Pt 2):285–293
  37. Stabile E., CD8+ T Lymphocytes Regulate the Arteriogenic Response to Ischemia by Infiltrating the Site of Collateral Vessel Development and Recruiting CD4+ Mononuclear Cells Through the Expression of Interleukin-16, 10.1161/circulationaha.105.576702
  38. Koponen Jonna K, Kekarainen Tuija, Heinonen Suvi E, Laitinen Anita, Nystedt Johanna, Laine Jarmo, Ylä-Herttuala Seppo, Umbilical Cord Blood–derived Progenitor Cells Enhance Muscle Regeneration in Mouse Hindlimb Ischemia Model, 10.1038/sj.mt.6300302
  39. Bonen Arend, The expression of lactate transporters (MCT1 and MCT4) in heart and muscle, 10.1007/s004210100516
  40. Dedkov E.I., Kostrominova T.Y., Borisov A.B., Carlson B.M., Resistance Vessel Remodeling and Reparative Angiogenesis in the Microcirculatory Bed of Long-Term Denervated Skeletal Muscles, 10.1006/mvre.2001.2372
  41. Kawai Kenichiro, Larson Barrett J., Ishise Hisako, Carre Antoine Lyonel, Nishimoto Soh, Longaker Michael, Lorenz H. Peter, Calcium-Based Nanoparticles Accelerate Skin Wound Healing, 10.1371/journal.pone.0027106
  42. Mendel DB, Laird AD et al (2000) Development of SU5416, a selective small molecule inhibitor of VEGF receptor tyrosine kinase activity, as an anti-angiogenesis agent. Anticancer Drug Des 15:29–41
  43. Menke Nathan B., Ward Kevin R., Witten Tarynn M., Bonchev Danail G., Diegelmann Robert F., Impaired wound healing, 10.1016/j.clindermatol.2006.12.005
  44. Creager MA, Loscalzo J (2008) Diseases of the extremities. In: Fauci AS, Braunwald E, Kasper DL (eds) Harrison’s principles of internal medicine, 17th edn. McGraw Hill, New-York, pp 1568–1570
  45. Dhup Suveera, Kumar Dadhich Rajesh, Ettore Porporato Paolo, Sonveaux Pierre, Multiple Biological Activities of Lactic Acid in Cancer: Influences on Tumor Growth,Angiogenesis and Metastasis, 10.2174/138161212799504902
  46. DIMMER Kai-Stefan, FRIEDRICH Björn, LANG Florian, DEITMER Joachim W., BRÖER Stefan, The low-affinity monocarboxylate transporter MCT4 is adapted to the export of lactate in highly glycolytic cells, 10.1042/0264-6021:3500219
  47. Hashimoto T., Hussien R., Oommen S., Gohil K., Brooks G. A., Lactate sensitive transcription factor network in L6 cells: activation of MCT1 and mitochondrial biogenesis, 10.1096/fj.07-8174com
  48. Porporato Paolo E., Dhup Suveera, Dadhich Rajesh K., Copetti Tamara, Sonveaux Pierre, Anticancer Targets in the Glycolytic Metabolism of Tumors: A Comprehensive Review, 10.3389/fphar.2011.00049
  49. Folkman Judah, Angiogenesis in cancer, vascular, rheumatoid and other disease, 10.1038/nm0195-27
  50. Dorrell Michael I., Aguilar Edith, Scheppke Lea, Barnett Faith H., Friedlander Martin, Combination angiostatic therapy completely inhibits ocular and tumor angiogenesis, 10.1073/pnas.0607542104
  51. CHANG Xiaotian, WEI Chao, Glycolysis and rheumatoid arthritis : Glycolysis and RA, 10.1111/j.1756-185x.2011.01598.x
  52. Barba Ignasi, Garcia-Ramírez Marta, Hernández Cristina, Alonso María Angeles, Masmiquel Lluis, García-Dorado David, Simó Rafael, Metabolic Fingerprints of Proliferative Diabetic Retinopathy: An1H-NMR–Based Metabonomic Approach Using Vitreous Humor, 10.1167/iovs.10-5348
  53. Shanmugasundaram Madhan, Ram Vinny K., Luft Ulrich C., Szerlip Molly, Alpert Joseph S., Peripheral Arterial Disease-What Do We Need to Know?, 10.1002/clc.20925
  54. Enerson Bradley E., Drewes Lester R., Molecular Features, Regulation, and Function of Monocarboxylate Transporters: Implications for Drug Delivery, 10.1002/jps.10389
  55. Cori CF, Cori GT (1929) Glycogen formation in the liver with d- and l-lactic acid. J Biol Chem 81:389–403
  56. Patel MS, Jomain-Baum M, Ballard FJ, Hanson RW (1971) Pathway of carbon flow during fatty acid synthesis from lactate and pyruvate in rat adipose tissue. J Lipid Res 12:179–191
  57. Pagliassotti MJ, Donovan CM (1990) Role of cell type in net lactate removal by skeletal muscle. Am J Physiol 258:E635–E642
  58. Fredenberg Susanne, Wahlgren Marie, Reslow Mats, Axelsson Anders, The mechanisms of drug release in poly(lactic-co-glycolic acid)-based drug delivery systems—A review, 10.1016/j.ijpharm.2011.05.049
Référence bibliographique Porporato, Paolo ; Payen, Valéry ; De Saedeleer, Christophe ; Préat, Véronique ; Thissen, Jean-Paul ; et. al. Lactate stimulates angiogenesis and accelerates the healing of superficial and ischemic wounds in mice.. In: Angiogenesis, Vol. 15, p. 581-592 (2012)
Permalien http://hdl.handle.net/2078.1/112257