Melanocortin 1 receptor agonist protects podocytes through catalase and RhoA activation

American Journal of Physiology - Renal Physiology

Volumn 310, Issue 9, 2016, Pages F846-F856

  Elvin, Johannes ^a   Buvall, Lisa ^a,b   Lindskog Jonsson, Annika ^a   Granqvist, Anna ^a   Lassén, Emelie ^a   Bergwall, Lovisa ^a   Nyström, Jenny ^a   Haraldsson, Börje ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Actin stress fiber; Melanocortin 1 receptor; Oxidative stress; Podocyte

Indexed keywords

CATALASE; MELANOCORTIN 1 RECEPTOR; MELANOCORTIN RECEPTOR AGONIST; PUROMYCIN AMINONUCLEOSIDE; REACTIVE OXYGEN METABOLITE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; ANTIMETABOLITE;

ACTIN FILAMENT; APOPTOSIS; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; OXIDATIVE STRESS; PODOCYTE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; STRESS FIBER; UPREGULATION; AGONISTS; ANIMAL; CELL CULTURE; CHEMICALLY INDUCED; DRUG EFFECTS; ENZYME ACTIVATION; GENETICS; METABOLISM; MOUSE; NEPHROSIS;

ANIMALS; ANTIMETABOLITES; CATALASE; CELLS, CULTURED; ENZYME ACTIVATION; MICE; NEPHROSIS; OXIDATIVE STRESS; PODOCYTES; PUROMYCIN AMINONUCLEOSIDE; REACTIVE OXYGEN SPECIES; RECEPTOR, MELANOCORTIN, TYPE 1; RHOA GTP-BINDING PROTEIN; STRESS FIBERS;

EID: 84984629951     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00231.2015     Document Type: Article

References (64)

1. Anwar S, Larson DS, Naimi N, Ashraf M, Culiberk N, Liapis H, Wei C, Reiser J, Brennan DC. A case report of adrenocorticotropic hormone to treat recurrent focal segmental glomerular sclerosis post-transplantation and biomarker monitoring. Front Med 2: 13, 2015.
2. Asanuma K, Yanagida-Asanuma E, Takagi M, Kodama F, Tomino Y. The role of podocytes in proteinuria. Nephrology 12: S15–S20, 2007.
3. Beaumont KA, Newton RA, Smit DJ, Leonard JH, Stow JL, Sturm RA. Altered cell surface expression of human MC1R variant receptor alleles associated with red hair and skin cancer risk. Hum Mol Genet 14: 2145–2154, 2005.
4. Beck LH, Bonegio RGB, Lambeau G, Beck DM, Powell DW, Cummins TD, Klein JB, Salant DJ. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N Engl J Med 361: 11–21, 2009.
5. Berg AL, Arnadottir M. ACTH-induced improvement in the nephrotic syndrome in patients with a variety of diagnoses. Nephrol Dial Transplant 19: 1305–1307, 2004.
6. Berg AL, Nilsson-Ehle P, Arnadottir M. Beneficial effects of ACTH on the serum lipoprotein profile and glomerular function in patients with membranous nephropathy. Kidney Int 56: 1534–1543, 1999.
7. Björnson A, Moses J, Ingemansson A, Haraldsson B, Sörensson J. Primary human glomerular endothelial cells produce proteoglycans, and puromycin affects their posttranslational modification. Am J Physiol Renal Physiol 288: F748–F756, 2005.
8. Bomback AS, Canetta PA, Beck LH Jr, Ayalon R, Radhakrishnan J, Appel GB. Treatment of resistant glomerular diseases with adrenocorticotropic hormone gel: a prospective trial. Am J Nephrol 36: 58–67, 2012.
9. Bomback AS, Tumlin JA, Baranski J, Bourdeau JE, Besarab A, Appel AS, Radhakrishnan J, Appel GB. Treatment of nephrotic syndrome with adrenocorticotropic hormone (ACTH) gel. Drug Design Dev Ther 5: 147–153, 2011.
10. Buvall L, Rashmi P, Lopez-Rivera E, Andreeva S, Weins A, Wallentin H, Greka A, Mundel P. Proteasomal degradation of Nck1 but not Nck2 regulates RhoA activation and actin dynamics. Nat Commun 4: 2863, 2013.
11. Catania A, Gatti S, Colombo G, Lipton JM. Targeting melanocortin receptors as a novel strategy to control inflammation. Pharmacol Rev 56: 1–29, 2004.
12. Chittiprol S, Chen P, Petrovic-Djergovic D, Eichler T, Ransom RF. Marker expression, behaviors, and responses vary in different lines of conditionally immortalized cultured podocytes. Am J Physiol Renal Physiol 301: F660–F671, 2011.
13. Daehn I, Casalena G, Zhang T, Shi S, Fenninger F, Barasch N, Yu L, D’Agati V, Schlondorff D, Kriz W, Haraldsson B, Bottinger EP. Endothelial mitochondrial oxidative stress determines podocyte depletion in segmental glomerulosclerosis. J Clin Invest 124: 1608–1621, 2014.
14. Faul C, Asanuma K, Yanagida-Asanuma E, Kim K, Mundel P. Actin up: regulation of podocyte structure and function by components of the actin cytoskeleton. Trends Cell Biol 17: 428–437, 2007.
15. Ferrer E, Juan-García A, Font G, Ruiz MJ. Reactive oxygen species induced by beauvericin, patulin and zearalenone in CHO-K1 cells. Toxicol In Vitro 23: 1504–1509, 2009.
16. Garcia-Borron JC, Sanchez-Laorden BL, Jimenez-Cervantes C. Melanocortin-1 receptor structure and functional regulation. Pigment Cell Res 18: 393–410, 2005.
17. Gong R. Leveraging melanocortin pathways to treat glomerular diseases. Adv Chronic Kidney Dis 21: 134–151, 2014.
18. Granqvist A, Nilsson UA, Ebefors K, Haraldsson B, Nyström J. Impaired glomerular and tubular antioxidative defense mechanisms in nephrotic syndrome. Am J Physiol Renal Physiol 299: F898–F904, 2010.
19. Greka A, Mundel P. Cell biology and pathology of podocytes. Annu Rev Physiol 74: 299–323, 2011.
20. Haraldsson B. A new era of podocyte-targeted therapy for proteinuric kidney disease. N Engl J Med 369: 2453–2454, 2013.
21. Haraldsson B, Nystrom J, Deen WM. Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev 88: 451–487, 2008.
22. Haraldsson B, Nyström J. The glomerular endothelium: new insights on function and structure. Curr Opin Nephrol Hypertens 21: 258–263, 2012.
23. Haraldsson BS. The endothelium as part of the integrative glomerular barrier complex. Kidney Int 85: 8–11, 2014.
24. Heasman SJ, Ridley AJ. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9: 690–701, 2008.
25. Henri P, Beaumel S, Guezennec A, Poumès C, Stoebner PE, Stasia MJ, Guesnet J, Martinez J, Meunier L. MC1R expression in HaCaT keratinocytes inhibits UVA-induced ROS production via NADPH oxidase- and cAMP-dependent mechanisms. J Cell Physiol 227: 2578–2585, 2012.
26. Herpin TF, Yu G, Carlson KE, Morton GC, Wu X, Kang L, Tuerdi H, Khanna A, Tokarski JS, Lawrence RM, Macor JE. Discovery of tyrosine-based potent and selective melanocortin-1 receptor small-molecule agonists with anti-inflammatory properties. J Med Chem 46: 1123–1126, 2003.
27. Hladunewich MA, Cattran D, Beck LH, Odutayo A, Sethi S, Ayalon R, Leung N, Reich H, Fervenza FC. A pilot study to determine the dose and effectiveness of adrenocorticotrophic hormone (H.P. Acthar gel) in nephrotic syndrome due to idiopathic membranous nephropathy. Nephrol Dial Transplant 29: 1570–1577, 2014.
28. Kadekaro AL, Kavanagh R, Kanto H, Terzieva S, Hauser J, Kobayashi N, Schwemberger S, Cornelius J, Babcock G, Shertzer HG, Scott G, Abdel-Malek ZA. α-Melanocortin and endothelin-1 activate antiapoptotic pathways and reduce dna damage in human melanocytes. Cancer Res 65: 4292–4299, 2005.
29. Kang L, McIntyre KW, Gillooly KM, Yang Y, Haycock J, Roberts S, Khanna A, Herpin TF, Yu G, Wu X, Morton GC, Tuerdi H, Koplowitz B, Walker SG, Wardwell-Swanson J, Macor JE, Lawrence RM, Carlson KE. A selective small molecule agonist of the melanocortin-1 receptor inhibits lipopolysaccharide-induced cytokine accumulation and leukocyte infiltration in mice. J Leukoc Biol 80: 897–904, 2006.
30. Kriz W, LeHir M. Pathways to nephron loss starting from glomerular diseases-insights from animal models. Kidney Int 67: 404–419, 2005.
31. Kummer S, Jeruschke S, Wegerich LV, Peters A, Lehmann P, Seibt A, Mueller F, Koleganova N, Halbenz E, Schmitt CP, Bettendorf M, Mayatepek E, Gross-Weissmann ML, Oh J. Estrogen receptor alpha expression in podocytes mediates protection against apoptosis in-vitro and in-vivo. PLos One 6: e27457, 2011.
32. Leoni G, Voisin MB, Carlson K, Getting SJ, Nourshargh S, Perretti M. The melanocortin MC1receptor agonist BMS-470539 inhibits leucocyte trafficking in the inflamed vasculature. Br J Pharmacol 160: 171–180, 2010.
33. Li X, Tao H, Xie K, Ni Z, Yan Y, Wei K, Chuang PY, He JC, Gu L. cAMP signaling prevents podocyte apoptosis via activation of protein kinase A and mitochondrial fusion. PLos One 9: e92003, 2014.
34. Lindberg BG, Merritt EA, Rayl M, Liu C, Parmryd I, Olofsson B, Faye I. Immunogenic and antioxidant effects of a pathogen-associated prenyl pyrophosphate in Anopheles gambiae. PLos One 8: e73868, 2013.
35. Lindskog A, Ebefors K, Johansson ME, Stefansson B, Granqvist A, Arnadottir M, Berg AL, Nystrom J, Haraldsson B. Melanocortin 1 receptor agonists reduce proteinuria. J Am Soc Nephrol 21: 1290–1298, 2010.
36. Lindskog Jonsson A, Granqvist A, Elvin J, Johansson ME, Haraldsson B, Nyström J. Effects of melanocortin 1 receptor agonists in experimental nephropathies. PLos One 9: e87816, 2014.
37. Ling LU, Tan KB, Lin H, Chiu GNC. The role of reactive oxygen species and autophagy in safingol-induced cell death. Cell Death Dis 2: e129, 2011.
38. Maresca V, Flori E, Bellei B, Aspite N, Kovacs D, Picardo M. MC1R stimulation by alpha-MSH induces catalase and promotes its re-distribution to the cell periphery and dendrites. Pigment Cell Melanoma Res 23: 263–275, 2010.
39. Margoliash E, Novogrodsky A, Schejter A. Irreversible reaction of 3-amino-1:2:4-triazole and related inhibitors with the protein of catalase. Biochem J 74: 339–348, 1960.
40. Mundel P, Heid HW, Mundel TM, Kruger M, Reiser J, Kriz W. Synaptopodin: an actin-associated protein in telencephalic dendrites and renal podocytes. J Cell Biol 139: 193–204, 1997.
41. Mundel P, Reiser J. Proteinuria: an enzymatic disease of the podocyte? Kidney Int 77: 571–580, 2010.
42. Nijenhuis T, Sloan AJ, Hoenderop JG, Flesche J, van Goor H, Kistler AD, Bakker M, Bindels RJ, de Boer RA, Moller CC, Hamming I, Navis G, Wetzels JF, Berden JH, Reiser J, Faul C, van der Vlag J. Angiotensin II contributes to podocyte injury by increasing TRPC6 expression via an NFAT-mediated positive feedback signaling pathway. Am J Pathol 179: 1719–1732, 2011.
43. Nimnual AS, Taylor LJ, Bar-Sagi D. Redox-dependent downregulation of Rho by Rac. Nat Cell Biol 5: 236–241, 2003.
44. Oh J, Reiser J, Mundel P. Dynamic (re)organization of the podocyte actin cytoskeleton in the nephrotic syndrome. Pediatr Nephrol 19: 130–137, 2004.
45. Picardi L, Villa G, Galli F, Piazza V, Bovio G, Efficace E, Montagna G, Semeraro L, Segagni S, Salvadeo A. ACTH therapy in nephrotic syndrome induced by idiopathic membranous nephropathy. Clin Nephrol 62: 403–404, 2004.
46. Pippin JW, Brinkkoetter PT, Cormack-Aboud FC, Durvasula RV, Hauser PV, Kowalewska J, Krofft RD, Logar CM, Marshall CB, Ohse T, Shankland SJ. Inducible rodent models of acquired podocyte diseases. Am J Physiol Renal Physiol 296: F213–F229, 2009.
47. Piwkowska A, Rogacka D, Jankowski M, Dominiczak MH, Stepinski JK, Angielski S. Metformin induces suppression of NAD(P)H oxidase activity in podocytes. Biochem Biophys Res Commun 393: 268–273, 2010.
48. Ponticelli C, Passerini P, Salvadori M, Manno C, Viola BF, Pasquali S, Mandolfo S, Messa P. A randomized pilot trial comparing methylprednisolone plus a cytotoxic agent versus synthetic adrenocorticotropic hormone in idiopathic membranous nephropathy. Am J Kidney Dis 47: 233–240, 2006.
49. Ransom RF, Lam NG, Hallett MA, Atkinson SJ, Smoyer WE. Glucocorticoids protect and enhance recovery of cultured murine podocytes via actin filament stabilization. Kidney Int 68: 2473–2483, 2005.
50. Rico M, Mukherjee A, Konieczkowski M, Bruggeman LA, Miller RT, Khan S, Schelling JR, Sedor JR. WT1-interacting protein and ZO-1 translocate into podocyte nuclei after puromycin aminonucleoside treatment. Am J Physiol Renal Physiol 289: F431–F441, 2005.
51. Robinson S, Dixon S, August S, Diffey B, Wakamatsu K, Ito S, Friedmann PS, Healy E. Protection against UVR involves MC1Rmediated non-pigmentary and pigmentary mechanisms in vivo. J Invest Dermatol 130: 1904–1913, 2010.
52. Schaldecker T, Kim S, Tarabanis C, Tian D, Hakroush S, Castonguay P, Ahn W, Wallentin H, Heid H, Hopkins CR, Lindsley CW, Riccio A, Buvall L, Weins A, Greka A. Inhibition of the TRPC5 ion channel protects the kidney filter. J Clin Invest 123: 5298–5309, 2013.
53. Segal PE, Choi MJ. Recent advances and prognosis in idiopathic membranous nephropathy. Adv Chronic Kidney Dis 19: 114–119, 2012.
54. Shankland SJ, Pippin JW, Reiser J, Mundel P. Podocytes in culture: past, present, and future. Kidney Int 72: 26–36, 2007.
55. Song X, Mosby N, Yang J, Xu A, Abdel-Malek Z, Kadekaro AL. α-MSH activates immediate defense responses to UV-induced oxidative stress in human melanocytes. Pigment Cell Melanoma Res 22: 809–818, 2009.
56. Szardenings M, Muceniece R, Mutule I, Mutulis F, Wikberg JE. New highly specific agonistic peptides for human melanocortin MC1 receptor. Peptides 21: 239–243, 2000.
57. Tian D, Jacobo SM, Billing D, Rozkalne A, Gage SD, Anagnostou T, Pavenstadt H, Hsu HH, Schlondorff J, Ramos A, Greka A. Antagonistic regulation of actin dynamics and cell motility by TRPC5 and TRPC6 channels. Sci Signal 3: ra77, 2010.
58. Tomas NM, Beck LH Jr, Meyer-Schwesinger C, Seitz-Polski B, Ma H, Zahner G, Dolla G, Hoxha E, Helmchen U, Dabert-Gay AS, Debayle D, Merchant M, Klein J, Salant DJ, Stahl RA, Lambeau G. Thrombospondin type-1 domain-containing 7A in idiopathic membranous nephropathy. N Engl J Med 371: 2277–2287, 2014.
59. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, Tamakawa H, Yamagami K, Inui J, Maekawa M, Narumiya S. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389: 990–994, 1997.
60. Vega-Warner V, Ransom RF, Vincent AM, Brosius FC, Smoyer WE. Induction of antioxidant enzymes in murine podocytes precedes injury by puromycin aminonucleoside. Kidney Int 66: 1881–1889, 2004.
61. Wada T, Pippin JW, Marshall CB, Griffin SV, Shankland SJ. Dexamethasone prevents podocyte apoptosis induced by puromycin aminonucleoside: role of p53 and Bcl-2-related family proteins. J Am Soc Nephrol 16: 2615–2625, 2005.
62. Wada T, Pippin JW, Nangaku M, Shankland SJ. Dexamethasone’s prosurvival benefits in podocytes require extracellular signal-regulated kinase phosphorylation. Nephron Exp Nephrol 109: e8–e19, 2008.
63. Yoo TH, Fornoni A. Nonimmunologic targets of immunosuppressive agents in podocytes. Kidney Res Clin Pract 34: 69–75, 2015
64. Yu H, Suleiman H, Kim AHJ, Miner JH, Dani A, Shaw AS, Akilesh S. Rac1 activation in podocytes induces rapid foot process effacement and proteinuria. Mol Cell Biol 33: 4755–4764, 2013.